Parasitic Lice Help to Fill in the Gaps of Early Hominid History Julie M. Allen, Cedric O. Worman, Jessica E. Light, and David L. Reed Introduction Hearing the word “lice” will immediately terrify parents and cause school nurses to spring into action. Pediculosis (a louse infestation) is not a new problem—lice have coevolved with humans over millions of years, and at this moment in human history, head lice are a worldwide epidemic. Although they can infect anyone, they are most common among children aged 3–12 and are widely spread throughout our school systems. According to the World Health Organization, it is thought that around 10–20 % of children are infested worldwide. In the USA alone, approximately 6–12 million infestations occur every year (Frankowski and Weiner 2002). Parents have attacked this problem using every method from shaving their child’s head to covering the entire scalp with petroleum jelly, vinegar, and even toxic chemicals like kerosene (Meinking 1999; Frankowski and Weiner 2002). Even though we have been evolving with lice for millions of years, we are still struggling to understand and eradicate these parasites. J.M. Allen (*) Florida Museum of Natural History, University of Florida, Museum Rd. and Newell Dr., Gainesville, FL 32611, USA e-mail: juliema@illinois.edu C.O. Worman Biology Department, University of Florida, 223 Bartram Hall, Gainesville, FL 32611, USA J.E. Light Department of Wildlife and Fisheries Sciences, Texas A&M University, 210 Nagle Hall, College Station, TX 77843, USA D.L. Reed Florida Museum of Natural History, University of Florida, Museum Rd. and Newell Dr., Gainesville, FL 32611, USA J.F. Brinkworth and K. Pechenkina (eds.), Primates, Pathogens, and Evolution, Developments in Primatology: Progress and Prospects 38, DOI 10.1007/978-1-4614-7181-3_6, © Springer Science+Business Media New York 2013 161 162 J.M. Allen et al. Fig. 1 Male human head louse (Pediculus humanus) left and female chimpanzee louse (Pediculus schaeffi) right. The circle outlines the modified tibia with extended claw for hanging onto and climbing up and down hair shafts Although it is the most common, the head louse (Pediculus humanus capitis) is just one of three types of lice that infest humans. Most similar to head lice are body lice (Pediculus humanus humanus), perhaps more aptly called “clothing lice” because they live principally in the clothing. The third and more distantly related louse is the pubic louse (Pthirus pubis), which lives primarily in the pubic region. Taxonomically, pubic lice belong to a different louse family, Phthiridae, whereas head and clothing lice belong to the family Pediculidae. These insects are hostspecific obligate parasites that do not spend any part of their life cycle off their host. They live around 30 days and females attach eggs to the base of a hair shaft, laying around 3–5 eggs per day. Eggs hatch in 5–9 days, and in about 10 days nymphs become reproductively active. These insects feed on the blood of their hosts several times a day (Buxton 1947). Because lice have secondarily lost their wings, they cannot fly. Instead, lice move by climbing up and down hair shafts. Their tibiae are modified with claws that are adapted specifically for holding onto hair (Fig. 1). If a louse is removed from its host for a long period of time, it does not survive. In fact, most lice become so dehydrated that they cannot move after 21 h off the host (Burgess 2004). Although we have been studying lice for hundreds of years (Darwin 1871; Hooke 1665), research slowed significantly in the 1940s when DDT was introduced and seemed likely to eradicate lice. In the 1990s, however, prevalence of lice increased worldwide due to pesticide resistance, and in 1997 there was a massive outbreak of typhus, which is transmitted by clothing lice (Raoult and Roux 1999), and louse research found a new beginning (Burgess 2004). This research reached a new peak in 2010 when the first louse genome (Pediculus humanus humanus) was sequenced (Kirkness et al. 2010). The genome work revealed a number of fascinating characteristics about lice. For example, clothing lice have the smallest insect genome sequenced to date (only 108 megabases), and they do not have many of the genes related to environmental sensing, which may be a result of their highly specialized lifestyle as an obligate parasite. Here we review the biology and latest research on head, clothing, and pubic lice including what these parasites can teach us about our own evolutionary history. Parasitic Lice Help to Fill in the Gaps of Early Hominid History 163 Head Lice: Pediculus humanus capitis Head lice have long been considered an economical and societal problem rather than a dangerous infectious disease (Hansen and O’Havier 2004; Stafford 2008). The estimated cost of head louse infestation ranges from $367 million to $1 billion per year. Spending on over-the-counter chemical treatments, loss of school days, and loss of workdays for parents contribute to this high cost (Hansen and O’Havier 2004; Frankowski and Bocchini 2010). There are a number of myths and stigmas associated with head lice that cause undue stress to parents and family members of children infested with lice (Frankowski and Weiner 2002; Gordon 2007; Frankowski and Bocchini 2010). For example, head lice can be found in all social classes and are not correlated with cleanliness (Frankowski and Bocchini 2010). Head lice do not appear to spread disease in natural populations. Although, some studies have detected infectious bacteria in head lice (Sasaki et al. 2006a,b; Bonilla et al. 2009; Angelakis et al. 2011 but see Parola et al. 2006), and other research has suggested that head lice even have the capacity to transmit the infectious bacteria (Goldberger and Anderson 1912; Murray and Torrey 1975) to date, there has not been a known outbreak of disease caused by head louse transmission. The most common symptom from a head louse infestation is pruritis (itching) caused by a bite from the louse. In extreme cases, scratching the bite can cause an infection from common skin bacteria (Meinking 1999), but for the most part head lice are a mere annoyance rather than a dangerous parasite. Manual removal of lice is a common means of treating head louse infestations, an activity which has shown up in artwork for centuries (the term “nit-picking” actually refers to the physical removal of lice). Recently, the most popular treatment of head lice has been chemical. Unfortunately, pesticide resistance has increased tremendously over the last few decades, (Burgess 2004) and in some places lice are even resistant to more than one chemical. Currently no pesticide is 100 % effective (Frankowski and Weiner 2002; Tebruegge et al. 2011). Other nonchemical methods (such as manual removal) have been suggested; however, these methods have been met with mixed success likely due to the effort required to remove all the lice (Frankowski and Bocchini 2010). One new method of louse eradication focuses on the temperature sensitivity of the lice. This sensitivity to temperature has been known for some time (Buxton 1947); in fact studies have shown that lice are likely to leave a person with a fever for a healthy person (Lloyd 1919 cited in Buxton 1947), and it has been suggested for some time that hot temperatures may be a way to kill lice. Following this literature, a modified prototype of the LouseBuster™ has recently been released. This appliance uses hot air to kill the lice by dehydrating them at high temperatures. In clinical trials, this method had a 94 % success rate in killing lice and 100 % success killing eggs on infected individuals. Thus, the LouseBuster™ may prove to be a faster, more effective, nonchemical method for treating head lice (Bush et al. 2011). Head lice are most commonly transmitted from human to human by direct contact (Canyon and Speare 2010). It has been long suggested that lice can be 164 J.M. Allen et al. transmitted via fomites, objects such as combs, and pillows (Burkhart and Burkhart 2007). However, this idea has been strongly challenged, and little to no evidence of fomite transmission has been found (Canyon and Speare 2010). Furthermore, head lice removed from the head die quickly due to dehydration (Burgess 2004), making fomite transmission unlikely. Unfortunately, methods to eradicate lice from schools have been difficult due to these types of misinformed ideas about how lice move from child to child. An extremely controversial societal issue with lice is the “no nit” policies adopted by some schools. These policies require children to stay out of school until they are free of detectable nits (louse eggs). One issue with this policy is that empty nit casings (those from which the louse has already hatched) can remain on the hair long after a louse outbreak has ended. Furthermore, eggs are incubated by body heat so nits more than 1 cm from the scalp are unlikely viable (Frankowski and Weiner 2002). This means that nits that are farther from the scalp are likely empty and left over from a cured infestation and may remain in the hair until it grows out. Even more problematic, there is evidence that cases of head lice are frequently misdiagnosed (Pollack et al. 2000). Because of this, many children, particularly those with longer hair, miss school unnecessarily (Gordon 2007), which inflates the total cost of pediculosis per year. Not only are these children missing valuable class time, they are likely to face bullying by their classmates upon return due to the stigma associated with head lice. Clothing Lice: Pediculus humanus humanus Clothing lice (Pediculus humanus humanus), which are also called body lice, live in clothing fibers where they attach eggs to cloth fibers rather than hair (Buxton 1947). They look very similar to head lice, although there are some important differences between them. Clothing lice are generally larger than head lice and can consume a larger blood meal (Busvine 1978; Meinking 1999; Reed et al. 2004). Clothing lice only go to the skin to feed a few times a day, much less than head lice and likely why they consume a larger blood meal. Additionally, unlike head lice, clothing lice are associated with conditions of poor hygiene and are commonly found on those forced to live in crowded situations where they lack the ability to change or wash clothes regularly such as refugees, the homeless, soldiers, and victims of war or natural disasters (Meinking 1999). It has been unclear for quite some time whether head lice and clothing lice are one species or two, and many studies have found conflicting results (Busvine 1978; Amevigbe et al. 2000; Burgess 2004; Leo and Barker 2005; Leo et al. 2005; Light et al. 2008). However, recent studies with more comprehensive sampling are finding that clothing lice and head lice are in fact the same species and that clothing lice evolve from head lice in certain conditions (such as in situations where individuals have a considerable head louse infestation and poor hygiene; Li et al. 2010). It is now clear that throughout our history clothing lice have opportunistically evolved Parasitic Lice Help to Fill in the Gaps of Early Hominid History 165 repeatedly from head lice to fill a different ecological niche from that of their head louse counterparts (Reed et al. 2004; Light et al. 2008; Li et al. 2010). Finally, and perhaps most importantly, clothing lice are the known vectors of three human pathogens: Rickettsia prowazekii (agent of epidemic typhus; Andersson and Andersson 2000), Borrelia recurrentis, and Bartonella quintana (the agents of relapsing fever and trench fever, respectively; Buxton 1947). These transmissions occur when louse feces are unintentionally rubbed into an open wound caused by the louse bite, most generally occurring when scratching the area of the bite (Buxton 1947). These diseases have had a devastating impact throughout human history. For example, epidemic typhus may have been largely responsible for the demise of Napoleon’s Grand Army around 1812 (Raoult et al. 2006). These diseases have been a problem not only historically but also recently. In 1999, a large outbreak of endemic typhus broke out in Burundi, infecting more than 100,000 people. With the growing worldwide problem of lice due to pesticide resistance, these diseases will need to be carefully monitored. Pubic Lice: Pthirus pubis The third type of louse that parasitizes humans is Pthirus pubis, commonly known as the “crab” or pubic louse. Pubic lice are a sexually transmitted disease (STD), and their presence has often been found in combination with other STD infections (Anderson and Chaney 2009). Pubic lice are also a worldwide phenomenon. Although it is much more difficult to calculate the level of prevalence because infections are not often reported, recent estimates suggest that 2 % of the world’s adult population are infected with pubic lice (Anderson and Chaney 2009). Pubic lice are found in all levels of society and among all ethnic groups (Meinking 1999). Pubic lice live primarily in the androgenic hairs (hair that begins to grow at sexual maturity) around the groin; however, these lice have been found on children in the eyelashes, eyebrows, and edges of the hairline. In rare cases the presence of Pthirus on children has alerted authorities to incidents of child abuse; however, this is not common (Chosidow 2000). It is thought that Pthirus prefer hair that is more widely spaced due to the wider spacing of their claws (Waldeyer 1900; Nuttall 1918; Fisher and Morton 1970). Interestingly, it is thought that fomite transmission is more important in pubic lice, which may explain how children get an infestation in their eyebrows and eyelashes without sexual contact (Meinking 1999). Similar to human head lice, pesticides and manual removal are considered to be the primary treatment for pubic lice (Orion et al. 2004). The genus Pthirus has two species of lice: the human pubic louse and the gorilla louse, Pthirus gorillae. The host associations of this genus of louse have puzzled researchers for some time: why are humans and gorillas, but not chimpanzees, parasitized by Pthirus? Furthermore, although lice are very host specific, why do humans have two genera of lice (Pediculus and Pthirus), whereas chimpanzees and gorillas each have one (Pediculus and Pthirus, respectively; Fig. 2)? In 2007, Reed et al. conducted molecular dating analyses on gorilla and human pubic lice and found that 166 J.M. Allen et al. Fig. 2 The coevolutionary history of humans (Homo), chimpanzees (Pan), and gorillas (Gorilla) and their lice. The primate lineages are indicated by thin black lines and black boxes that depict the longevity (box height) and the species richness (box width) of the primate genera known from physical evidence (either the fossil record or extant species). Parasite lineages are indicated with thick gray bars with the lighter gray representing Pediculus and the darker gray Pthirus. Dotted lines indicate possible coevolutionary scenarios that remain unclear due to lack of data. The most recent estimated divergence between gorillas and the lineage leading to humans and chimpanzees is shown at 9.2 mya; however, we also show the possible divergence (and consequently the cospeciation event) between these lineages at 13 mya incorporating the gorilla-like fossil Chororapithecus abyssinicus (dashed lines at 13 mya). We further show the host switch event 3–4 mya by lice in the genus Pthirus from the gorilla lineage onto the hominin lineage. The extinct hominin genus Paranthopus and its possible association with both Pediculus and Pthirus are shown at approximately 2 mya. Events on the right represent our current knowledge of hominin history including time ranges for the origin of clothing use by Homo sapiens, the first putative shelters, the earliest known butcher marks, and the development of bipedality (as indicated from the louse data). Asterisks mark isolated fossil finds. Species abbreviations are as follows: Ar. ka = Ardipithecus kaddaba, Ar. ra = Ardipithecus ramidus, Au. ana = Australopithecus anamensis, Au. afa = Australopithecus afarensis, and Au. afr = Australopithecus africanus. O = Orrorin tugenensis, S = Sahelanthropus tchadensis, K = Kenyanthropus platyops, and A = Australopithecus bahrelghazali. (1) McBrearty and Jablonski (2005). (2) Foley (2002). (3) Pickford et al. (1988). (4) Suwa et al. (2007). (5) Strait et al. (1997). (6) Leakey et al. (2001). (7) Brunet et al. (1995). (8) Kimbel et al. (2006). (9) WoldeGabriel et al. (2009). (10) Haile-Selassie (2001). (11) Pickford et al. (2002). (12) Brunet et al. (2002). (13) Toups et al. (2011). (14) Rantala (1999). (15) McPherron et al. (2010). (16) Reed et al. (2007). (17) Pickford et al. (2002) Parasitic Lice Help to Fill in the Gaps of Early Hominid History 167 these two species were sister taxa. Additionally, these two taxa diverged only 3–4 million years ago (mya), much more recently than the gorilla/human-chimp split, which is estimated at around 9 mya (Wilkinson et al. 2011). This finding was extremely interesting as it shed light onto two details of human evolutionary history that were previously unknown. Here we go into more detail about the biology of Pthirus to discuss what this host switch tells us about our ancestors 3–4 mya. Lice Tell Us About Our Past Sucking lice have been coevolving with their hosts for at least the last 65 million years and likely much longer (Light et al. 2010). Due to their obligate nature and the fact that they mostly move between hosts via direct contact, these blood-feeding lice have been used to give us clues about their hosts’ evolutionary history not easily gleaned from the fossil record (e.g., behavior). Interestingly, this idea dates back to Darwin (1871) who in On the Decent of Man wrote: “…and the fact of races of man being infested with parasites which appear to be specifically distinct might fairly be urged as an argument that the races themselves ought to be classed as distinct species.” Although the idea that races of humans represent different species is no longer entertained and even the concept of race has dramatically changed since Darwin’s time, the idea that lice can tell us about our evolutionary history is now well accepted and gaining momentum (Whiteman and Parker 2005; Hypsa 2006; Nieberding and Olivieri 2007; Reed et al. 2009). In 2003, it became apparent upon genetic examination of recently collected human head and clothing lice that there were several distinct lineages of lice (Kittler et al. 2003). Reed et al. (2004) used fossil calibrations for the split between humans and chimpanzees (5.6 mya) and the split between great apes and Old World monkeys (22.5 mya) to estimate the divergence time between these human louse lineages. They found that the youngest of these lineages splits around 1.18 mya, which is similar in age to the ancestor of Homo sapiens and H. neanderthalensis. The other louse lineage is even older, suggesting its origin may date back to a H. erectus-like host. Because head lice are primarily transmitted through direct contact, this finding suggests that modern humans came into contact with archaic hominin species and picked up distinct lineages of head lice. Although we do not know which archaic humans our ancestors came into contact with, the timing of the divergence of the ancient head louse lineages is consistent with contact with H. neanderthalensis and H. erectus. Furthermore, while the type of contact between different hominin species is unknown, recent work sequencing the H. neanderthalensis genome found evidence of interbreeding between H. neanderthalensis and H. sapiens (Green et al. 2010; Yotova et al. 2011). Similar types of contact between H. sapiens and H. erectus would have been sufficient for the transfer of lice and may explain the existence of ancient lineages of head lice on modern humans. 168 J.M. Allen et al. Because clothing lice live exclusively in the clothing, they are thought to have evolved only after humans began to wear clothes, and it has long been proposed that dating the origin of clothing lice could give us a date by which H. sapiens must have been wearing clothing (Kittler et al. 2003, 2004). Previous estimates of when humans started wearing clothing were based on the emergence of eyed needles (which suggests complex clothing had already been developed) around 40,000 mya (Delson et al. 2000) and sometime after the loss of body hair as late as 1.2 mya (Rogers et al. 2004; based on molecular evidence) and as early as 3 mya (Reed et al. 2007; detailed below). Recent molecular evidence from clothing lice suggests that clothing use originated between 83,000 and 170,000 years ago, which is earlier than previously proposed, and suggests that clothing use by H. sapiens likely originated before they moved out of Africa (Toups et al. 2011). This clothing use may have enabled modern humans to more readily move into colder climates as they migrated out of Africa and eventually throughout the world. The coevolutionary relationships between great apes and their lice have been worked out morphologically and molecularly and are illustrated in Fig. 2. Humans and chimpanzees share lice in the genus Pediculus as sister taxa, and humans and gorillas share lice in the genus Pthirus (Fig. 2). The split between human and chimpanzee lice was estimated to be 5–7 mya (Reed et al. 2004, using mitochondrial genes; Light et al. 2008, using a multigenic approach with mitochondrial and nuclear genes), strongly suggesting cospeciation between these two lice and their primate hosts (humans and chimpanzees also are believed to have diverged at this time; Wilkinson et al. 2011). On the other hand, Reed et al. (2007) found that the Pthirus and Pediculus are sister taxa and they diverged ~13 mya, long before the presumed 7 mya split between gorillas and the other African apes (Fig. 2). Reed et al. (2007) hypothesized an evolutionary scenario in which there was a louse duplication (or speciation) event on the African ape common ancestor to humans, chimpanzees, and gorillas. In other words, one louse species would have diverged into two on the ape common ancestor. More recent refinement of the somewhat troublesome great ape molecular clock has pushed the gorilla divergence back to 9.2 mya (Wilkinson et al. 2011). Additionally, a recent fossil find of the gorilla-like ape Chororapithecus abyssinicus dating to 10–11 mya (Suwa et al. 2007) suggests that the great ape molecular clock may still be underestimating the divergence of the gorillas by millions of years. If true, the presumed louse duplication event ~13 mya suggested by Reed et al. (2007) could have actually been a cospeciation event, suggesting that the divergence time between gorillas and the other African apes occurred ~13 mya, far earlier than currently thought (Fig. 2). Reed et al. (2007) also examined the history of the two species of Pthirus, one on gorillas and the other on humans, which diverged 3–4 mya. Reed et al. (2007) hypothesized that after Pthirus and Pediculus diverged ~13 mya, the Pthirus lineage remained on ancestral gorillas but went extinct on the common ancestor of humans and chimpanzees, and the Pediculus lineage remained on the common ancestor of humans and chimpanzees but went extinct on ancestral gorillas. Then, approximately 3–4 mya, the Pthirus lineage from ancestral gorillas switched to a human ancestor (Fig. 2). This type of host switch is not uncommon; there have been a Parasitic Lice Help to Fill in the Gaps of Early Hominid History 169 number of zoonotic transmissions of diseases from primates, as well as domesticated animals, to humans (Wolfe et al. 2007). For example, HIV-1 is now known to have come from a chimpanzee (Gao et al. 1999) possibly as a result of humans hunting chimpanzees for food. This particular host-switching event of Pthirus on ancestral gorillas to our human ancestors gives us clues about human evolutionary history that we outline and detail below. Human Hair Loss Reed et al. (2007) postulated that a Pthirus-type louse switched hosts from archaic gorillas to hominins approximately 3–4 mya. It is interesting to consider what was necessary for this host switch to have been successful: there had to have been a niche for Pthirus to occupy. Studies of chewing lice have found that their mouthparts (which grip the hair) are highly adapted and specialized to the hair of their hosts (Reed et al. 2000), so it is likely that hair type is similarly important to sucking lice. Rather than using their mouthparts to grip hair, sucking lice use their claws, which are also highly specialized. Pthirus, in particular, is highly adapted to hairs in the pubic regions as these hairs are more widely spaced, which match the wider spacing of their claws (see below). As stated previously, pubic hair is a type of androgenic hair—hair that grows in response to increased levels of androgens circulating in the human body at sexual maturity (Randall 2008). Proposed functions of pubic hair (pheromonal and visual signaling; Randall 2008) could have only come into play after the loss of typical ape body hair. Additionally, the invasion of a new host would have been far more likely if Pediculus had already been confined to the head by the loss of functional body hair, leaving competitorfree regions available to Pthirus. We hypothesize that the loss or reduction of body hair as well as the development of androgenic hair would have facilitated the success of this host switch and therefore suggest that human hair loss and the gain of androgenic hair had occurred by 3–4 mya, a date that is much older than other predictions. Among primates, humans are unique in their apparent nakedness. Humans, however, are not actually hairless. They have a similar number and density of hair follicles as other great apes, but the hairs are much finer (i.e., smaller in diameter) and shorter and offer little protection or insulation (Kushlan 1985; Amaral 1996; Rantala 1999). There is a great variety of hypotheses ranging from the bizarre to the pedestrian as to why humans had such a drastic reduction in body hair (reviewed in Rantala 2007). Many of these hypotheses are directly related to the Pthirus host switch because they either incorporate habitat (as discussed below) and thermodynamics (which is closely tied to habitat) or attempt to establish the timing of hair reduction. Habitat and thermodynamics are important to the cooling device, bipedality, hunting, vestiary, allometry, and other hypotheses of why humans lost their body hair. The timing of hair loss is incorporated to some extent in any hair loss hypothesis, but it is particularly important in the clothing, vestiary, and ectoparasite hypotheses. 170 J.M. Allen et al. The reduction in body hair has obvious thermodynamic consequences. This loss of insulation increases heat exchange with the environment. Several body hair loss hypotheses (see Rantala 2007) are based on the need to shed increased heat loads resulting from either a move from forest into hotter savanna habitats (cooling device, bipedality, hunting, vestiary hypotheses), an increased activity (hunting and vestiary hypotheses), or a large body size (allometry hypothesis). The cooling device hypothesis states that the increased heat load was simply caused by the move into open savannas from the forest (Rantala 2007). The bipedality hypothesis adds to this by examining how an upright stance decreases the solar heat load experienced by an individual in a bipedal stance compared to a quadrupedal stance (Wheeler 1992). Active hunting in the savanna and the excess heat that must be shed from high levels of activity are incorporated into the hunting hypothesis (Brace and Montagu 1977). The additional need to retain heat during the cool savanna nights (fulfilled by the use of clothing) while being able to shed heat during the day, presumably through hairlessness and sweating, is the basis of the vestiary hypothesis (Kushlan 1985). The allometry hypothesis is based on the observation that larger primates have increasingly more widely spaced hair (Schwartz and Rosenblum 1981). As intuitive as it may seem to people from cooler climes that shedding insulation increases heat loss, hot open savanna environments make body hair extremely valuable for decreasing heat gain from both solar radiation and the air (Newman 1970). The upright stance central to the bipedality hypothesis reduces solar heat gain compared to a quadrupedal stance, making it less detrimental to be hairless, but it does not make hair loss beneficial in savanna environments (Amaral 1996). In addition, it is now clear that bipedalism evolved in basal hominins by the time of Orrorin tugenensis (Pickford et al. 2002; Galik et al. 2004) around 5.7–6 mya (Richmond and Jungers 2008), long before the shift to dry open habitats by Homo (Elton 2008), and that evaporative cooling is not prevented by body hair; the patas monkey (Erythrocebus patas), a cursorial savanna monkey, has both thick fur and effective sweating (Mahoney 1980). Another characteristic of savannas compared to forests (addressed by the vestiary hypothesis) is colder nights unmitigated by heat-retaining forest tree cover and humidity (Amaral 1996). This makes the insulation provided by body hair even more valuable and makes loss of body hair in the savanna environment doubly detrimental. The allometry hypothesis is not a complete explanation of human hairlessness by itself. Schwartz and Rosenblum (1981) reanalyzed Schultz’s (1931, 1969) measurements of primate hair density and found that there are fewer hairs per unit of body surface in larger primates compared to smaller primates. They reasoned that this reduction in body hair was likely due to thermoregulatory constraints associated with decreasing ratios of surface area to volume, which make shedding metabolic heat difficult for larger animals. Because fossil data indicated that early australopithecine hominins weighed between 45 and 70 kg (Pilbeam and Gould 1974), Schwartz and Rosenblum (1981) hypothesized that substantial decreases in hominin hair density likely occurred prior to human shifts from forest to grassland habitats at the end of the Pliocene. Parasitic Lice Help to Fill in the Gaps of Early Hominid History 171 However, the effective hairlessness of humans is not just a result of hair density but also hair size. In contrast to humans, other similar-sized and larger apes (orangutans and gorillas) have substantial body hair. Thus, hominins appear to have exaggerated the typical primate strategy of shedding metabolic heat via reduced insulative effectiveness of body hair (the heavy sweating of humans and patas monkeys does not appear to be typical of primates; Amaral 1996) by reducing hair size. It seems likely that this was in answer to an additional metabolic heat load beyond that experienced by typical apes. Although it is impossible to say with any degree of certainty what this additional heat load was, the development of bipedalism, a more energetically efficient mode of locomotion than knuckle walking (Sockol et al. 2007), hints that increased daily travel may have been important to the basal hominin niche and that hair loss may have occurred very early on. The extra metabolic heat produced by travel through forests could have been shed by decreasing body hair insulation without the costs of nakedness associated with savanna environments. Based on the timing of the Pthirus host switch, the habitat in which this switch likely occurred (see below), and the problems of hairlessness in open habitats, hair loss in the hominin line almost certainly occurred in a forested habitat and was complete and effectively irreversible by the time savanna habitats were fully utilized. The human dependence on sweating as a cooling mechanism likely occurred long after hair loss to deal with the additional heat loads in open habitats as sweating is less effective in the humid still air of forests than in drier more open habitats (Newman 1970; Montagna 1972). Other than lice, the only line of evidence that helps establish the timing of hair loss in the hominin line is genetic. The human melanocortin 1 receptor (MC1R) gene is involved in human skin coloration. By looking at the neutral variation in this gene, Rogers et al. (2004) estimated that human skin has been exposed to strong sunlight for at least 1.2 my. Therefore, based on the MC1R data, human ancestors became both hairless and began living in the savanna between 1.2 mya and 6–7 mya (the chimpanzee/hominin split). The lice data are consistent with the MC1R data but give a narrower range of 3–4 mya from the Pthirus switch to the 6–7 million year split between the human and chimpanzee lineages. The timing of hair loss is particularly central to the clothing, vestiary, and ectoparasite hypotheses. The clothing hypothesis (Glass 1966) is similar to the vestiary hypothesis (Kushlan 1985) in that they both posit that clothing superseded the insulative value of body hair and hair loss occurred with or after the invention of clothing. However, while the vestiary hypothesis holds (erroneously, as discussed above) that the loss of body hair was advantageous during the hot days and that clothing replaced the need for body hair during the cool nights, the clothing hypothesis argues that after clothing was invented, body hair disappeared as it was no longer needed (Glass 1966; however, Glass does not propose a reason for the invention and use of clothing by hominins with functional coats of body hair). The louse and MC1R data estimates for both hairlessness (Pthirus, >3–4 mya in Reed et al. 2007; MC1R, >1.2 mya in Rogers et al. 2004) and the invention of clothing (Pediculus, 0.08–0.17 mya in Toups et al. 2011) indicate that clothing had nothing to do with the evolution of hairlessness in hominins. 172 J.M. Allen et al. The ectoparasite hypothesis states that when hominins first established long-term habitations, they were beset with new types of ectoparasites, such as fleas, that completed their life cycles in the living space but off the body of the host (Rantala 1999). Thus, the loss of body hair was a defense against increased parasite loads encouraged by the establishment of a home base. In apparent conflict with the adaptationagainst-ectoparasites hypothesis is the presence of pubic hair (Pagel and Bodmer 2003). Pubic hair, however, may play an important role in sexual selection and thus may have been selected for in spite of its ability to shelter ectoparasites. The moist and humid environment of the pubic region (due to an increased density of sweat glands; Stoddart 1990) is favorable to pheromonal signaling (Guthrie 1976), and pubic hair could have initially functioned in pheromonal signaling (Randall 1994), visual signaling (Randall 2008), or both. Rantala (1999) associates the beginnings of long-term settlements with an increase in cooperative hunting and places both developments at ~1.8 mya based on excavations of Homo habilis artifacts at Olduvai Gorge. While this estimate is consistent with the hairlessness range provided by the MC1R gene (>1.2 mya), it is far later than the hairlessness estimate provided by the Pthirus host switch. Pediculus and Pthirus The two genera of human lice (Pediculus and Pthirus) occupy distinct niches on the body (head/clothing and pubic region, respectively). Many researchers have wondered why Pediculus and Pthirus do not co-occur and are apparently isolated to these different regions especially given their similar biology (Howlett 1917). Hypotheses have included Pthirus having a preference for darkness and moist areas (Nuttall 1918; however, this idea is not accepted as Pthirus survives on eyelashes and eyebrows) and that differences in hair spacing have geographically restricted these lice because Pediculus cannot adequately grasp the hairs of the pubic region, and Pthirus cannot grasp the hairs on the head. Both genera of lice have been found occasionally occupying and surviving in other regions of the body (see below), but they do not seem to be successful in these areas. Of these hypotheses, hair spacing seems to be the most likely explanation for restricting these two types of lice to their respective habitats. Schwartz and Rosenblum (1981) found that there are fewer hairs per unit of body surface in larger primates compared to smaller primates. If the Reed et al. (2007) hypothesis that the human pubic louse (Pthirus pubis) is a descendent of gorilla lice is true, then based on Schwartz and Rosenblum’s (1981) findings, we can postulate that Pthirus was adapted to living among widely spaced hairs because gorillas are the largest extant primate. Early studies of Pthirus support this idea. Pthirus uses its second and third pair of legs to cling to host hair, and these legs, when stretched apart, span a distance of 2 mm (Waldeyer 1900; Nuttall 1918; Fisher and Morton 1970). It just so happens that hairs in the pubic region are also distributed 2 mm apart (Waldeyer 1900; Nuttall 1918). Furthermore, the number of hairs present in Parasitic Lice Help to Fill in the Gaps of Early Hominid History 173 the pubic region (34 hairs/cm2) is significantly less than the head (220 hairs/cm2; Waldeyer 1900; Payot 1920). All in all, Pthirus appears to prefer body regions with widely spaced hairs for better grasping as well as for ease of flattening itself against the skin (Burgess et al. 1983; Burgess 1995; Nuttall 1918; Buxton 1947; Fisher and Morton 1970). According to measurements made by Schultz (1931), chimpanzee hair density is more similar to humans than to gorillas. That, in addition to the lack of pubic-type hair on chimpanzees, may help explain why there are no Pthirus species currently parasitizing chimpanzees. The Pthirus preference for widely spaced hairs is likely why this genus can be occasionally found in other sparsely haired areas on the human body, such as the margins of the scalp, eyebrows, eyelashes, and areas of the trunk such as the chest, stomach, and thighs (if sufficient body hair is present; Burgess 1995, and references therein; Buxton 1941, 1947; Elgart and Higdon 1973). Pediculus, in comparison, is rarely found in the pubic region of humans (Busvine 1944). Pediculus schaeffi, the louse on chimpanzees louse, is more catholic in habitat choice than Pediculus humanus and can be found almost anywhere on a chimpanzee host but favors the groin, underarms, and head (D. Cox, pers. comm.). It is likely that the Pediculus found on hominins before the loss of body hair was similarly widely spread but was restricted to the head region during the hominin denudation and subsequently prevented from spreading to androgenic hair because the larger spacing of pubic hair made movement from one hair to another difficult. Differences in mobility also may prevent Pediculus from traveling to the pubic region as often as Pthirus appears to move to other parts of the body. Although several studies have found that Pediculus moves faster than Pthirus when displaced from the body (Nuttall 1918; Busvine 1944), Pthirus does tend to wander more (Burgess et al. 1983). Furthermore, head lice are recognized as being rather picky in how they move from hair to hair, suggesting that they are unlikely to move readily to foreign objects or fomites (Canyon et al. 2002). Closer examination of the first tarsal claws (which may facilitate movement when lice are not in contact with hair) of both Pediculus and Pthirus reveals why there may be differences in mobility between these two genera (Ubelaker et al. 1973). The inner surface of the first tarsal claw in Pthirus is serrated, allowing for traction even on smooth surfaces, whereas in Pediculus the inner surface of the claw is smooth and the lice are unable to move without hair follicles or roughened surfaces (Nuttall 1918; Ubelaker et al. 1973; Burkhart and Burkhart 2000). This simple difference, along with preferential movement patterns, may restrict Pediculus from moving easily on smooth, non-haired substrates. Pthirus, on the other hand, with their serrated first tarsal claws, may be able to move much more easily on non-haired substrates, thus allowing them to reach other parts of the body such as the perimeter of the scalp. The biology of these two parasites supports the idea that human ancestors had not only lost their body hair by the host switch 3–4 mya (isolating Pediculus in the head region) but that early hominins had also developed androgenic hair, providing a suitable environment for Pthirus. 174 J.M. Allen et al. Habitats of Early Hominins Given the fossil species currently known, the most parsimonious scenario explaining the appearance of Pthirus in the human lineage is a host switch directly from gorilla ancestors to human ancestors. This scenario strongly implies that the two ancestral host species came into repeated and close contact, which further implies significant overlap in habitat. By combining data from the fossil record, paleoclimate, extant species, and the Pthirus host switch, we can augment the current thinking of the habitat and habits of human ancestors. The fossil record of nonhuman African apes is abysmal to say the least. There is currently only one known chimpanzee fossil, which lived 0.5 mya (McBrearty and Jablonski 2005); one gorilla fossil from 5 to 6 mya (Pickford et al. 1988); and the very gorilla-like Chororapithecus abyssinicus from 10 to 11 mya (Suwa et al. 2007; Fig. 2). The reasons for the dearth of these fossils are likely due to several factors (Cote 2004). For one, apes were an uncommon component of the fauna in any region, and African fossil sites commonly produce fewer specimens than Eurasian fossil sites. Therefore, a site must produce a large number of fossils if any apes are expected to be represented in the first place. Second, with the exceptions of Samburupithecus kiptalami and Nakalipithecus nakayami, which might have been adapted to drier forests (Kunimatsu et al. 2007), nonhuman African apes are, and appear to always have been, tightly associated with moist tropical forests. The wet acidic soil in these types of habitats is much more conducive to quick bone decomposition than fossilization, so it is likely that very few specimens were fossilized to begin with (Kingston 2007). Added to those problems is the fact that sites currently under moist tropical forests are seldom found or excavated, partly due to a lack of exposed strata and partly due to the political insecurity that often inflames those regions, reducing safety for international teams and handicapping intranational capacity for, and interest in, research. It is generally thought that the nonhuman African apes are conservative in body form and habits contrasting with the hominins that stumbled upon a new behavior/ body form (bipedalism) that led to their subsequent radiation into a speciose and relatively diverse group. That assumption is supported by the dearth of non-hominin ape fossils in Africa, which indicates they were restricted to the wet forests that are particularly hostile to fossil formation (Kingston 2007), and by the nature of the few fossils that have been found. Additionally, the morphology and wear of the Chororapithecus abyssinicus fossil from 11 to 10 mya (Suwa et al. 2007) and the gorilla tooth from 5 to 6 mya (Pickford et al. 1988), as well as their respective faunal assemblage contexts, suggest that gorillas have been conservative in diet and habitat over the period of time during which the hominin group was rapidly developing novel traits and habits. Molecular work has also indicated the conservatism of the gorilla lineage. Thalmann et al. (2007) have estimated that eastern and western gorillas (Gorilla beringei and G. gorilla, respectively) diverged 0.9–1.6 mya with very little subsequent gene flow between those two species. Thalmann et al. (2007) also suggest that Parasitic Lice Help to Fill in the Gaps of Early Hominid History 175 the genetic divergence between the eastern and western forms is small enough to unite the two into a single species. The gene flow between the two groups is low enough that it is likely not the cause of their genetic similarity but a result of it. With the apparent conservatism of the gorilla lineage in mind, we can cautiously use the natural history of extant gorillas to inform us of the probable habits of their ancestors and examine how that information fits into and expands the understanding of our ancestors. Gorillas today range across forested tropical Africa (with a large interruption between the eastern and western species) from lowland rainforest to high-altitude montane forest. In spite of these wide longitudinal and altitudinal ranges, both species share similar diets based on succulent herbaceous vegetation (Kingdon 1974). The diet often incorporates more fruit in areas where fruit is available, but herbaceous vegetation still forms a large portion of the diet, retaining its primary importance especially as a fallback food in times of fruit scarcity (Yamagiwa and Basabose 2006). The importance of fibrous herbaceous foods makes gorillas more independent of often unreliably fruiting trees than the two chimpanzee species (Pan troglodytes and P. paniscus); however, it also limits their available habitat to moist forests with enough sunlight penetrating the canopy to support a rank herbaceous understory (Schaller 1963). While swidden agriculture produces ample areas of lush secondary growth, prior to agriculture, suitable gorilla foraging areas would have been limited to montane forests, river edges, treefall gaps, elephant tramples, and the like (Schaller 1965a), with feeding and use by gorillas likely slowing succession and extending the usable life and possibly the size of temporary clearings (Plumptre 1994). Even if the gorilla lineage had significantly different dietary preferences than extant gorillas during the host switch of Pthirus 3–4 mya, it is unlikely that the differences would have a meaningful impact on our analysis as the conservatism of body and tooth form and lack of fossils indicate a folivorous/frugivorous diet in a moist forest. During the 3–4 mya range given for the Pthirus host switch, there were 1–4 hominin species present (Fig. 2) depending on the validities of species identifications: Australopithecus anamensis, A. afarensis, A. bahrelghazali, and Kenyanthropus platyops (Fig. 2). K. platyops (3.5 mya) is known from only one locality and the skull upon which the identification is based is severely fragmented and distorted (Leakey et al. 2001). Therefore, the identity of the specimen as a new genus (Kenyanthropus), a new species within Australopithecus, or another A. afarensis specimen is controversial (White 2003; Spoor et al. 2010). However, if K. platyops is a valid species, it is potentially ancestral to both Homo and Paranthropus (robust australopithecines) and lived in a well-watered forest or woodland (Leakey et al. 2001; Strait and Grine 2004). Australopithecus bahrelghazali is another species known only from a single fossil from 3.5 mya (Brunet et al. 1995; Brunet 2010) and, like K. platyops, is controversial as to whether it is a separate species or an unusual A. afarensis (Kimbel et al. 2006; Guy et al. 2008). This is a unique find because it is the only australopithecine found in Chad rather than East or Southern Africa. Unfortunately, the state of the 176 J.M. Allen et al. fossils makes establishing phylogenetic relationships difficult (Strait and Grine 2004), but it is likely that A. bahrelghazali lived in a gallery forest/wooded savanna/ grassland mosaic context (Brunet et al. 1995). Australopithecus anamensis (3.9–4.2 mya) was probably the anagenetic ancestor of A. afarensis (Kimbel et al. 2006) and therefore also an ancestor of Homo (Strait et al. 1997). Because A. anamensis and A. afarensis are chronospecies, they appear to be similar in habitat and diet. The habitat of A. anamensis was likely mosaic forest, woodland, grassland, bush, and riverine forest (Bonnefille 2010). In spite of the variety of habitats postulated, A. anamensis seems to have been tied to the presence of at least some trees and lived at a time of increasing tree cover in Africa (Bonnefille 2010). The diet has been postulated with many methods. Tooth morphology suggests hard brittle items (Grine et al. 2006) but with the ability to exploit fleshy fruits (Teaford and Ungar 2000). Microwear patterns suggest tough and fibrous foods (Ungar et al. 2010). Finally, enamel microstructure suggests tough, hard, and abrasive foods with limited brittle and acidic foods (Macho and Shimizu 2010). It seems likely that the majority of the A. anamensis diet was fibrous vegetation that required grinding with brittle foods forming an important fallback food (Ungar et al. 2010). The fourth species, Australopithecus (Praeanthropus) afarensis, is by far the best understood of the four candidates and a presumed ancestor of Homo (Strait et al. 1997). Sites containing A. afarensis fossils have been found all over East Africa, which dated from 3.0 to 3.6 mya (Kimbel and Delezene 2009). The paleoenvironments of these sites, temporally and spatially, are extremely variable, ranging from steppe to woodland to forest (Bonnefille et al. 2004), but not wet dense evergreen forest (Bonnefille 2010). Because A. afarensis showed no apparent association with any particular habitat in a single site that fluctuated between being dominated by steppe and being dominated by forest, it has been described as a generalist (Bonnefille et al. 2004). The teeth of A. afarensis are thought to be adapted for crushing hard, brittle foods such as seeds, hard fruits, and/or tubers (Luca et al. 2010); however, microwear analysis of the teeth paints a different picture entirely. Compared to a variety of other primates, including those that specialize in eating hard seeds and those that consume substantial numbers of tubers, the microwear patterns on A. afarensis teeth from a diversity of habitats actually most closely resemble those of the mountain gorilla (Grine et al. 2006), the least frugivorous gorilla subspecies (Yamagiwa and Basabose 2006). As Grine et al. (2006) make clear, this resemblance does not mean that A. afarensis had the same diet as a gorilla, and the gross tooth morphology makes it unlikely that they could eat the same foods in the same way. Rather, the similarity means that they both ate fibrous foods with fine abrasiveness but none of the hard brittle foods for which the A. afarensis teeth appear to be adapted, at least not in the period before each of the individuals died. However, in areas of range overlap, it seems likely that they may have often been attracted to some of the same types of food, increasing the chances of interaction. The tooth morphology seemingly at odds with wear patterns may indicate a difference between commonly eaten preferred foods and the ability to efficiently process seasonally important fallback foods (Ungar 2004). Other authors suggest that Parasitic Lice Help to Fill in the Gaps of Early Hominid History 177 wetland vegetation was an important A. afarensis food (also exploited by gorillas in certain areas) that could explain the tooth wear patterns and the insensitivity of A. afarensis to changes in upland habitat (Verhaegen et al. 2002). Significant for this discussion is an additional A. afarensis food: meat scavenged from large animals with the help of stone butchering tools (McPherron et al. 2010). It is difficult to choose the hominin most likely to have first acquired Pthirus given the similarities between the hominins alive 3–4 mya and the limited, vague, and contradictory information available. However, the species with the most information available, A. afarensis, appears to be a good candidate because it was a habitat generalist that foraged on fibrous foods and scavenged large mammals (and therefore could have come into repeated contact with gorilla ancestors, as discussed below) and is a likely ancestor to Homo. However, nothing rules out other species in hominin lineage, especially as use of wet forests would not be recorded in the fossil record. Whichever hominin species was actually first infested with Pthirus, the successful transfer of a disease or parasite to another species is most likely when there is relatively frequent contact between the two host species, which indicates that moist forests were a far more important hominin habitat than previously realized. The savanna/grassland model of the origin of bipedalism and hominins has been largely rejected by careful examination of the context of hominin fossils (WoldeGabriel et al. 1994; Reed 1997; WoldeGabriel et al. 2009; Luca et al. 2010; Brunet 2010). These fossils tend to indicate the importance of wooded habitats including woodlands and dry forests or at the very least forests lining bodies of water or forest/ woodland/savanna/grassland mosaics (although mosaics can be an illusion created by the coarse resolution of the paleontological record and time averaging of more homogenous habitats changing over a period of time; Elton 2008). Though the emphasis has shifted from the savanna to the woodland and dry forest, moist forests have largely been ignored as potentially important habitats for hominins; however, there is no reason to think hominins would be less flexible in habitat use than those extant primates that use both wet forests and drier open habitats (Elton 2008). This oversight has certainly been reasonable based on the context of fossil finds; in fact, there has never been a hominin fossil found associated with rain forest habitat, more likely due to the difficulty of fossilization rain forests (Kingston 2007 and see above) than habitat specificity. However, the evidence of habitual contact between hominins and gorilla ancestors given by the Pthirus host switch provides strong support for wet forests playing a more important role in hominin evolution than normally thought. Additionally, the loss of body hair that is likely to have occurred before the Pthirus switch from gorilla ancestors to human ancestors is much more likely to have happened under a closed canopy forest than in a less wooded ecosystem because the forest reduces the usefulness of body hair by reducing the solar heat load and mitigating diurnal temperature changes as discussed above (Newman 1970). Thus, the loss of body hair likely occurred when hominins were restricted exclusively to dense forests long before the evolution of the australopithecines as habitat generalists that incorporated more open areas into their ranges. While 178 J.M. Allen et al. australopithecines could presumably still utilize warm moist forests, use of montane forests of australopithecines is not likely given the loss of body hair by this point and the cold temperatures experienced in these forests. Unfortunately, fossil evidence of wet forest use by hominins will likely be as difficult to come by as fossil evidence of the other great apes that are restricted to wet forests. As mentioned before, the fossil record is almost silent even on the subject of common chimpanzees, which venture into drier habitats (such as woodlands and scrublands) than gorillas but remain largely tied to closed canopy forests. Thus, if restricted to fossil evidence, our picture of hominin evolution and habits is severely limited by the taphonomic processes in the moist forests that form the origin of African ape diversity. Our suggestion that australopithecines expanded their habitat from drier wooded areas into wet tropical forests introduces several more possibilities. Habitat use could have been seasonal with australopithecines predictably moving from drier habitats to wet forest areas and back. Alternately, a widely spread generalist species, as A. afarensis has been proposed to be, might have populations permanently inhabiting entirely different habitats. In this case, the question becomes which habitat was preferred, i.e., which, if any, was able to support higher densities of hominins. A third possibility is that one of the habitats was primary with the other being utilized only in times of drought, etc. The importance of moist forests with poor fossilization conditions to hominins raises the possibility that it was not the dry woodlands that were the center of hominin radiation; rather the radiation occurred in the rain forests with a minority of the species expanding out into more xeric areas to be fossilized and finally found. If this is true, we may still be missing a large portion of hominin diversity. Of course, for Pthirus to have switched hosts successfully, sharing habitats would have been insufficient for transfer—far more intimate contact would have been required. However, the contact would not have to be as intimate as most people seem to gleefully assume. Although hybrids between different guenon monkey species are known (Struhsaker et al. 1988; de Jong and Butynski 2010), there are far more likely scenarios than two species as divergent as archaic gorillas and australopithecines having sexual contact. Pthirus are known to be transmitted via fomites (Meinking 1999) and therefore could have potentially switched hosts if a hominin used an abandoned louse-infested archaic gorilla nest (Reed et al. 2007). All extant great apes including orangutans fashion nests (Schaller 1965b), so it is reasonable to assume that all apes 3–4 mya also made nests. While this scenario is possible, it seems unlikely. Great ape nests (aside from those of humans) are constructed swiftly for a single use and are simple rudimentary structures. This is especially true for gorilla nests made on the ground, which have better rims than bottoms, provide little if any padding, and are typically constructed in 1 min (though the minority that are made in the trees are more substantial; Schaller 1965a). Unfortunately (but not unexpectedly), there is no surviving evidence of australopithecine nests or nest use. However, if they practiced the single-use pattern typical of great apes, there would have been little reason for individuals who did not reuse their own nests to reuse the nests of another species. Parasitic Lice Help to Fill in the Gaps of Early Hominid History 179 On the other hand, if australopithecines reused nests like at least some of the later Homo spp., the reuse would probably have been motivated by increased effort required to build more complex and functional structures. Again, the reuse of old slipshod gorilla-type nests would have been unlikely. A more probable scenario for contact between human and gorilla ancestors is the existence of mixed foraging groups. Though rare compared to multiple species associations in monkeys (Yamagiwa and Basabose 2006), mixed foraging groups have been observed containing gorillas and chimpanzees. Interactions from avoidance (Yamagiwa et al. 1996) to obliviousness (Kuroda et al. 1996) have been seen taking place in mixed groups of apes (even from a distance of 3 m; Stanford 2006). The nature of the interaction likely depends on food availability and level of competition as well as the individual personalities of those involved. Habituated gorilla and chimpanzee troops tend to ignore human observers, but some physical interactions (e.g., playing, bluffing, and testing) have occurred, normally with young animals. In primate mixed foraging groups, interactions are most frequent between young animals and can involve play. Mixed foraging groups of gorilla and human ancestors would have given opportunities for the Pthirus switch through play or grooming; however, primate interspecific interactions are rare even where multispecies associations are common. Aggressive interactions are the most numerous interactions, with play being relatively unusual and grooming being extremely rare and of short duration (Ihobe 1990; Heymann and Buchanan-Smith 2000). Because juveniles are typically the age group involved in interspecific interactions and young hominins would have not yet developed the pubic hair that forms the current habitat of Pthirus on humans, the ancestral lice would have to be passed to an adult host before they could become established on the new host species. The possibility of a host switch through mixed foraging groups does exist, but because aggression and play rarely involve physical contact (Rose 1977), which occurs quickly and generally between juveniles who would then have to pass Pthirus to an adult host, social interaction is a less likely route of host switching than the last possibility: the consumption of archaic gorilla meat by human ancestors. Other than the gorillas, all the African great apes hunt and consume meat, although only humans have managed to prey on animals of similar and larger body sizes through the use of relatively sophisticated tools. Given the body size of A. afarensis (♀, ~29 kg; ♂, ~45 kg; McHenry 1994) compared to that of gorillas (♀, ~80 kg; ♂, ~169 kg; Smith and Jungers 1997) as well as the dangerous nature of enraged gorillas and relatively simple tools used by the australopithecines, it seems unlikely that hunting archaic gorillas by early hominins would be a particularly effective or common food acquisition strategy. It is far more likely that scavenging on gorilla carcasses led to the kind of contact most conducive to a louse host switch: repeated close contact over a substantial period of time. Additionally, lice are extremely sensitive to environmental conditions and readily abandon dead hosts. The desperate situation of lice on a dead or dying host makes the switch to any available host, even one of the incorrect species, much more likely than casual contact between a living native host and a potential novel host. 180 J.M. Allen et al. The presence of likely butcher marks on the bones of large mammals contemporary with A. afarensis indicates that scavenging was likely an important and effective component in their feeding repertoire (McPherron et al. 2010, 2011; but see Domínguez-Rodrigo et al. 2010, 2011). Although the validity of these butcher marks does not determine the level of carnivory by A. afarensis (DomínguezRodrigo et al. 2010), simple tools would have enabled both more efficient processing of meat than allowed by primate dentition alone and the transportation of meat away from the main carcass to a location with less predation danger. Thus, the most likely scenario is that a hominin habitually used moist tropical forests far more than previously realized or shown by the fossil record and opportunistically scavenged meat from gorilla carcasses. This feeding resulting in contact with Pthirus that was frequent enough to establish a population of Pthirus on hominins 3–4 mya. Conclusion There has been much research into the biology, epidemiology, and the evolutionary history of lice. These parasites have bedeviled human and nonhuman primates alike for millions of years, and the increase in louse prevalence over the last 20 years suggests they will continue to parasitize humans for some time yet. Due to their obligate host-specific nature, we can use these parasites to inform us about human evolutionary history and gather information that is not available in the host fossil record, providing an unexpected benefit to an otherwise bothersome parasite. Although most great ape lice have strictly cospeciated with their great ape hosts, Pthirus pubis (the human pubic louse) has a different evolutionary history. Pthirus switched to the human lineage 3–4 mya from an archaic gorilla. The biology of Pthirus suggests that for this host switch to have occurred, suitable habitat had to be available, which indicates that hominins had not only lost their body hair but also developed androgenic hair by 3–4 mya. Because gorillas are conservative in their habitats and diet, we postulate that this likely means that these archaic hominins were using similar habitat as gorillas (moist forest habitat). The best candidate for this host switch was Australopithecus afarensis (based on our current knowledge). A. afarensis possibly butchered large mammal carcasses during this time, presenting a scenario of A. afarensis scavenging archaic gorilla meat and Pthirus likely switching to A. afarensis from a dead gorilla host. Pthirus then continued to evolve with the hominin lineage as a sexually transmitted disease due to their placement on the body, explaining the presence of two genera of lice (Pthirus and Pediculus) on extant humans today. Parasitic Lice Help to Fill in the Gaps of Early Hominid History 181 References Amaral LQ (1996) Loss of body hair, bipedality and thermoregulation: comments on recent papers in the journal of human evolution. J Hum Evol 30:357–366 Amevigbe MDD, Ferrer A, Champorie S, Monteny N, Deunff J, Richard-Lenoble D (2000) Isoenzymes of human lice: Pediculus humanus and P. capitis. Med Vet Entomol 14:419–425 Anderson AL, Chaney E (2009) Pubic lice (Pthirus pubis): history, biology and treatment vs. knowledge and beliefs of US college students. Int J Environ Res Public Health 6:592–600 Andersson JO, Andersson SG (2000) A century of typhus, lice and Rickettsia. Res Microbiol 151:143–150 Angelakis E, Rolain JM, Raoult D, Brouqui P (2011) Bartonella Quintana in head louse nits. FEMS Immunol Med Mic 62(2):244–246 Bonilla DL, Kabeya H, Henn J, Kramer VL, Kosoy MY (2009) Bartonella quintana in body lice and head lice from homeless persons, San Francisco, California, USA. Emerg Infect Dis 15(6):912–915 Bonnefille R (2010) Cenozoic vegetation, climate changes and hominid evolution in tropical Africa. Glob Planet Change 72:390–411 Bonnefille R, Potts R, Chalié F, Jolly D, Peyron O (2004) High-resolution vegetation and climate change associated with Pliocene Australopithecus afarensis. Proc Natl Acad Sci 101:12125–12129 Brace CL, Montagu A (1977) Human evolution, 2nd edn. Macmillan, New York Brunet M (2010) Two new Mio-Pliocene Chadian hominids enlighten Charles Darwin’s 1871 prediction. Phil Trans Roy Soc B 365:3315–3321 Brunet M, Beauvilain A, Coppens Y, Heintz E, Moutaye AHE, Pilbeam D (1995) The first australopithecine 2,500 kilometers west of the Rift Valley (Chad). Nature 378:273–275 Brunet M, Guy F, Pilbeam D, Mackaye HT, Likius A, Ahounta D, Beauvilain A, Blondel C, Bocherensk H, Boisserie J-R, De Bonis L, Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G, Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Mahamat A, Merceron G, Mouchelin G, Otero O, Campomanes PP, De Leon MP, Rage J-C, Sapanetkk M, Schusterq M, Sudrek J, Tassy P, Valentin X, Vignaud P, Viriot L, Zazzo A, Zollikofer C (2002) A new hominid from the Upper Miocene of Chad, Central Africa. Nature 418:145–151 Burgess IF (1995) Human lice and their management. Adv Parasitol 36:271–342 Burgess IF (2004) Human lice and their control. Annu Rev Entomol 49:457–481 Burgess I, Maunder JW, Myint TT (1983) Maintenance of the crab louse, Pthirus pubis, in the laboratory and behavioral studies using volunteers. Community Med 5:238–241 Burkhart CN, Burkhart CG (2000) The route of head lice transmission needs enlightenment for proper epidemiologic evaluations. Int J Dermatol 39(11):878–879 Burkhart CN, Burkhart CG (2007) Fomite transmission in head lice. J Am Acad Dermatol 56:1044–1047 Bush SE, Rock AN, Jones SL, Malenke JR, Clayton DH (2011) Efficacy of the LouseBuster, a new medical device for treating head lice (Anoplura: Pediculidae). J Med Entomol 48(1):67–72 Busvine JR (1944) Simple experiments on the behaviour of body lice (Siphunculata). Proc Roy Ent Soc Lond 19:22–26 Busvine JR (1978) Evidence from double infestations for the specific status of human head lice and body lice (Anoplura). Syst Entomol 3:1–8 Buxton PA (1941) On the occurrence of the crab-louse (Phthirus pubis: Anoplura) in the hair of the head. Parasitology 33:117–118 Buxton P (1947) The louse an account of the lice which infest man, their medical importance and control. Edward-Arnold, London Canyon DV, Spearce R, Muller R (2002) Spatial and kinetic factors for the transfer of head lice (Pediculus capitis) between hairs. J Invest Dermatol 119:629–631 Canyon DV, Speare R (2010) Indirect transmission of head lice via inanimate objects. Open Dermatol J 4:72–76 182 J.M. Allen et al. Chosidow O (2000) Scabies and pediculosis. Lancet 355:819–826 Cote SM (2004) Origins of the African hominoids: an assessment of the palaeobiogeographical evidence. CR Palevol 3:323–340 Darwin C (1871) The descent of man and selection in relation to sex, 2nd edn. John Murray, London de Jong YA, Butynski TM (2010) Thre Sykes’s Monkey Cercopithecus mitis × Vervet Monkey Chlorocebus pygerythrus hybrids in Kenya. Primat Cons 25:43–56 Delson E, Tattersall I, Van Couvering J, Brooks A (2000) Encyclopedia of human evolution and prehistory. Garland, New York Domínguez-Rodrigo M, Pickering TR, Bunn HT (2010) Configurational approach to identifying the earliest hominin butchers. Proc Natl Acad Sci 107(49):20929–20934 Domínguez-Rodrigo M, Pickering TR, Bunn HT (2011) Reply to McPherron et al.: Doubting Dikika is about data, not paradigms. Proc Natl Acad Sci 108(21):E117 Elgart ML, Higdon RS (1973) Pediculosis pubis of the scalp. Arch Dermatol 107:916–917 Elton S (2008) The environmental context of human evolutionary history in Eurasia and Africa. J Anat 212:377–393. Fisher I, Morton RS (1970) Phthirus pubis infestation. Br J Vener Dis 46:326–329 Foley R (2002) Adaptive radiations and dispersals in hominin evolutionary ecology. Evol Anthropol Suppl 1:132–137 Frankowski BL, Bocchini JA (2010) Head lice. Pediatrics 126:392–403 Frankowski BL, Weiner LB (2002) Head lice. Pediatrics 110(3):638–643 Galik K, Senut B, Pickford M, Gommery D, Treil J, Kuperavage AJ, Eckhardt RB (2004) External and internal morphology of the BAR 1002’00 Orrorin tugenensis femur. Science 305(5689):1450–1453 Gao, F, Bailes E, Robertson DL, Chen Y, Rodenburg CM, Michael SF, Cummins LB, Arthur LO, Peeters M, Shaw GM, Sharp PM, Hahn, BH (1999) Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436–441 Glass B (1966) The evolution of hairlessness in man. Science 152:294 Goldberger J, Anderson JF (1912) The transmission of typhus fever, with especial reference to transmission by the head louse (Pediculus capitis). Public Health Rep 27(9):297–307 Gordon SC (2007) Shared vulnerability: a theory of caring for children with persistent head lice. J School Nurs 5:283–292 Green RE, Krause J, Briggs AW, Maricic T, Stenzel U, Kricher M, Patterson N, Li H, Zhai W, Fritz MH, Hansen NF, Durand EY, Malaspinas A, Jensen JD, Marques-Bonet T, Alkan C, Prüfer K, Meyer M, Burbano HA, Good JM, Schultz R, Aximu-Petri A, Butthof A, Höber B, Höffner B, Siegemund M, Weihmann A, Nusbaum C, Lander ES, Russ C, Novod N, Affourtit J, Egholm M, Verna C, Rudan P, Brajkovic D, Kucan Z, Gušic I, Doronichev VB, Golovanova LV, Lalueza-Fox C, Rasilla M, Fortea J, Rosas A, Schmitz RW, Johnson PLF, Eichler EE, Falush D, Birney E, Mullikin JC, Slatkin M, Nielsen R, Kelso J, Lachmann M, Reich D, Pääbo S (2010) A draft sequence of the Neanderthal genome. Science 328:710–722 Grine FE, Ungar P, Teaford MF, El-Zaatari S (2006) Molar microwear in Praeanthropus afarensis: evidence for dietary stasis through time and under diverse paleoecological conditions. J Hum Evol 51 Guthrie RD (1976) Body hot spots: the anatomy of human social organs and behavior. Van Nostrand Reinhold, New York Guy F, Mackaye H-T, Likius A, Vignaud P, Schmittbuhl M, Brunet M (2008) Symphyseal shap variation in extant and fossil hominoids, and the symphysis of Australopithecus bahrelghazali. J Hum Evol 55:37–47 Haile-Selassie Y (2001) Late Miocene hominids from the Middle Awash, Ethiopia. Nature 412:178–181 Hansen RC, O’Havier JO (2004) Economic considerations associated with Pediculus humanus capitis infestation. Clin Ped 43:523–527 Heymann EW, Buchanan-Smith HM (2000) The behavioral ecology of mixed-species troops of callitrichine primates. Biol Rev 75:169–190 Parasitic Lice Help to Fill in the Gaps of Early Hominid History 183 Hooke R (1665) Micrographia: or some physiological description of minute bodies made by magnifying glasses with observations and inquiries thereupon. Council Royal Society of London for Improving of Natural Knowledge, London Howlett FM (1917) Notes on head- and body-lice and upon temperature reactions of lice and mosquitoes. Parasitology 10:186–188 Hypsa V (2006) Parasite histories and novel phylogenetic tools: alternative approaches to inferred parasite evolution from molecular markers. Int J Parasitol 36:141–155 Ihobe H (1990) Interspecific interactions between wild pygmy chimpanzees (Pan paniscus) and red colobus (Colobus badius). Primates 31:109–112 Kimbel WH, Delezene LK (2009) “Lucy” redux: a review of research on Australopithecus afarensis. Yearbk Phys Anthropol 52:2–48 Kimbel W, Lockwood CA, Ward CV, Leakey MG, Rak Y, Johanson DC (2006) Was Australopithecus anamensis ancestoral to A. afarensis? A case of anagenesis in the hominin fossil record. J Hum Evol 51:134–152 Kingdon J (1974) East African mammals: an altas of evolution in Africa. University of Chicago Press, Chicago Kingston JD (2007) Shifting adaptive landscapes: progress and challenges in reconstructing early hominid environments. Yearbk Phys Anthropol 50:20–58 Kirkness EF, Haas BJ, Sun W, Braig HR, Perotti MA, Clark JM et al (2010) Genome sequences of the human body louse and its primary endosymbiont provide insights into the permanent parasitic lifestyle. Proc Natl Acad Sci 107(27):12168–12173 Kittler R, Kayser M, Stoneking M (2003) Molecular evolution of Pediculus humanus and the origin of clothing. Curr Biol 13:1414–1417 Kittler R, Kayser M, Stoneking M (2004) Erratum molecular evolution of Pediculus humanus and the origin of clothing. Curr Biol 14:2309 Kunimatsu Y, Nakatsukasa M, Sawada Y, Sakai T, Hyodo M, Hyodo H, Itaya T, Nakaya H, Saegusa H, Mazurier A, Saneyoshi M, Tsujikawa H, Yamamoto A, Mbua E (2007) A new late Miocene great ape from Kenya and its implications for the origins of African great apes and humans. Proc Natl Acad Sci 104:19220–19225 Kuroda S, Nishihara T, Suzuki S, Oko RA (1996) Sympatric chimpanzees and gorillas in the Ndoki Forest, Congo. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 71–81 Kushlan JA (1985) The vestiary hypothesis of human hair reduction. J Hum Evol 14:29–32 Leakey MG, Spoor F, Brown FH, Gathogo PN, Kairie C, Leakey LN, McDougall I (2001) New hominin genus from eastern Africa shows diverse middle Pliocene lineages. Nature 410:433–440 Leo NP, Barker SC (2005) Unravelling the origins of the head lice and body lice of humans. Parasitol Res 98:44–47 Leo NP, Hughes JM, Yang X, Poudel SKS, Brogdon WG, Barker SC (2005) The head and body lice of humans are genetically distinct (Insecta: Phthiraptera: Pediculidae): evidence from double infestations. Heredity 95:34–40 Li W, Ortiz G, Fournier P-E, Gimenez G, Reed DL, Pittendrigh B et al (2010) Genotyping of human lice suggests multiple emergences of body lice from local head louse populations. PLoS Neglect Trop Dis 4(3):e641 Light JE, Toups MA, Reed DL (2008) What’s in a name: the taxonomic status of human head and body lice. Mol Phylogenet Evol 47(3):1203–1216 Light JE, Smith VS, Allen JM, Durden LA, Reed DL (2010) Evolutionary history of mammalian sucking lice (Phthiraptera: Anoplura). BMC Evol Biol 10:292 Lloyd L (1919) Lice and their menace to man. Frowde, Oxford Luca F, Perry GH, Di Rienzo A (2010) Evolutionary adaptations to dietary changes. Annu Rev Nutr 30:291–314 Macho GA, Shimizu D (2010) Kinematic parameters inferred from enamal microstructure: new insights into the diet of Australopithecus anamensis. J Hum Evol 58:23–32 Mahoney SA (1980) Cost of locomotion and heat balance during rest and running from 0 to 55°C in a patas monkey. J Appl Physiol: Respirat Environ Exercise Physiol 49:789–800 184 J.M. Allen et al. McBrearty S, Jablonski NG (2005) First fossil chimpanzee. Nature 437:105–108 McHenry H (1994) Behavioral ecological implications of early hominid body size. J Hum Evol 27:77–87 McPherron SP, Alemseged Z, Marean CW, Wynn JG, Reed D, Geraads D, Bobe R, Béarat HA (2010) Evidence for stone-tool-assisted consumption of animal tissues before 3.39 million years ago at Dikika, Ethiopia. Nature 466:857–860 McPherron SP, Alemseged Z, Marean C, Wynn JG, Reed D, Geraads D, Bobe R, Bearat H (2011) Tool-marked bones from before the Oldowan change the paradigm. Proc Natl Acad Sci 108(21):E116 Meinking TL (1999) Infestations. Curr Probl Dermatol 11(3):75–118 Montagna W (1972) The skin of nonhuman primates. Am Zool 12:109–121 Murray ES, Torrey SB (1975) Virulence of Rickettsia prowazeki for head lice. Ann N Y Acad Sci 266:25–34 Newman RW (1970) Why man is such a sweaty and thirsty naked mammal: a speculative review. Hum Biol 42:12–27 Nieberding CM, Olivieri I (2007) Parasites: proxies for host genealogy and ecology? Trends Ecol Evol 22:156–165 Nuttall GHF (1918) The Biology of Phthirus pubis. Parasitology 10:383–405 Orion E, Matz H, Wolf R (2004) Ectoparasitic sexually transmitted diseases: scabies and pediculosis. Clin Dermatol 22:513–519 Pagel M, Bodmer W (2003) A naked ape would have few parasites. Proc Roy Soc Lond B Biol 270:S117–S119 Parola P, Fournier PE, Raoult D (2006) Bartonella quintana, lice, and molecular tools. J Med Entomol 43(5):787 Payot F (1920) Contribution a l’etude du Phthirus pubis. Bull Soc Vaud Sci Nat 53:127–161 Pickford M, Senut B, Ssemmanda I, Elepu D, Obwona P (1988) Premiers resultats de la mission de l’Uganda palaeontology expedition a Nkondo (Pliocene du bassin du lac Albert, Ouganda). CR Acad Sci II 306:315–320 Pickford M, Senut B, Gommery D, Treil J (2002) Bipedalism in Orrorin tugenensis revealed by its femora. Comptes Rendus Palevol 1(4):191–203 Pilbeam D, Gould SJ (1974) Size and scaling in human evolution. Science 186:892–901 Plumptre AJ (1994) The effects of trampling damage by herbivores on the vegetation of the Parc National des Volcans, Rwanda. Afr J Ecol 32:115–129 Pollack RJ, Kiszewski AE, Spielman A (2000) Overdiagnosis and consequent mismanagement of head louse infestations in North America. Pediatr Infect Dis J 19(8):689–693 Randall VA (1994) Androgens and human hair growth. Clin Endocrinol 40:439–457 Randall VA (2008) Androgens and hair growth. Dermatol Ther 21:314–328 Rantala MJ (1999) Human nakedness: adaptation against ectoparasites? Int J Parasitol 29: 1987–1989 Rantala MJ (2007) Evolution of nakedness in Homo sapiens. J Zool 271:1–7 Raoult D, Roux V (1999) The body louse as a vector of reemerging human diseases. Clin Infect Dis 29:888–911 Raoult D, Dutour O, Houhamdi L, Jankauskas R, Fournier P-E, Ardagna Y et al (2006) Evidence for louse-transmitted diseases in soldiers of Napoleon’s Grand Army in Vilnius. J Infect Dis 193:112–120 Reed KE (1997) Early hominid evolution and ecological change through the African PlioPleistocene. J Hum Evol 32:289–322 Reed DL, Hafner MS, Allen SK (2000) Mammalian hair diameter as a possible mechanism for host specialization in chewing lice. J Mammal 81:999–1007 Reed DL, Smith VS, Hammond SL, Rogers AR, Clayton DH (2004) Genetic analysis of lice supports direct contact between modern and archaic humans. PLoS Biol 2(11):e340 Reed DL, Light JE, Allen JM, Kirchman JJ (2007) Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol 5:7 Parasitic Lice Help to Fill in the Gaps of Early Hominid History 185 Reed DL, Toups MA, Light JE, Allen JM, Flannigan S (2009) Lice and other parasites as markers of primate evolutionary history. In: Huffman M, Chapman C (eds) Primate parasite ecology: the dynamics and study of host-parasite relationships. Cambridge University Press, Cambridge, pp 231–250 Richmond BG, Jungers WL (2008) Orrorin tugenensis femoral morphology and the evolution of hominin bipedalism. Science 319:1662–1665 Rogers AR, Iltis D, Wooding S (2004) Genetic variation at the MC1R locus and the time since loss of body hair. Curr Anthropol 45:105–108 Rose MD (1977) Interspecific play between free ranging guerezas (Colobus guereza) and vervet monkeys (Cercopithecus aethiops). Primates 18:957–964 Sasaki T, Poudel SKS, Isawa H, Hayashi T, Seki N, Tomita T, Sawabe K, Kobayashi M (2006a) First molecular evidence of Bartonella quintana in Pediculus humanus capitis (Phthiraptera: Pediculidae, collected from Nepalese children. J Med Entomol 43(1):110–112 Sasaki T, Poudel SKS, Isawa H, Hayashi T, Seki N, Tomita T, Sawabe K, Kobayashi M (2006b) First molecular evidence of Bartonella quintana in Pediculus humanus capitis (Phthiraptera: Pediculidae), collected from Nepalese children. J Med Entomol 43(5):788 Schaller GB (1963) The Mountain Gorilla: ecology and behavior. University of Chicago Press, Chicago Schaller GB (1965a) The behavior of the Mountain Gorilla. In: DeVore I (ed) Primate behavior: field studies of monkeys and apes. Holt, Rinehart, and Winston, New York, pp 324–367 Schaller GB (1965b) Behavioral comparisons of the apes. In: DeVore I (ed) Primate behavior: field studies of monkeys and apes. Holt, Rinehart, and Winston, New York, pp 474–481 Schultz AH (1931) The density of hair in primates. Hum Biol 3:303–321 Schultz AH (1969) The life of primates. Universe Books, New York Schwartz GG, Rosenblum LA (1981) Allometry of hair density and the evolution of human hairlessness. Am J Phys Anthropol 55:9–12 Smith RJ, Jungers WL (1997) Body mass in comparative primatology. J Hum Evol 32:523–559 Sockol MD, Raichlen DA, Pontzer H (2007) Chimpanzee locomotor energetics and the origin of human bipedalism. Proc Natl Acad Sci 104:12265–12269 Spoor F, Leakey MG, Leakey LN (2010) Hominin diversity in the Middle Pliocene of eastern Africa: the maxilla of KNM-WT 40000. Proc Roy Soc Lond B 365:3377–3388 Stanford CB (2006) The behavioral ecology of sympatric African apes: implications for understanding fossil hominoid ecology. Primates 47:91–101 Stafford (2008) Head lice: evidence-based guidelines based on the Stafford Report 2008 Update. Public Health Med Environ Group Stoddart DM (1990) The scented ape: the biology and culture of human odour. Cambridge University Press, Cambridge Strait DS, Grine FE (2004) Inferring hominoid and early hominid phylogeny using craniodental characters: the role of fossil taxa. J Hum Evol 47:399–452 Strait DS, Grine FE, Moniz MA (1997) A reappraisal of early hominid phylogeny. J Hum Evol 32:17–82 Struhsaker TT, Butynski TM, Lwanga JS (1988) Hybridization between redtail (Cercopithecus ascanius schmidti) and blue (C. mitis stuhlmanni) monkeys in the Kibale Forest, Uganda. In: Gautier-Hion A, Bourlière F, Gautier JP, Kingdon J (eds) A primate radiation: evolutionary biology of the African Guenons. Cambridge University Press, Cambridge, pp 477–497 Suwa G, Kono RT, Katoh S, Asfaw B, Beyene Y (2007) A new species of great ape from the late Miocene epoch in Ethiopia. Nature 448:921–924 Teaford MF, Ungar PS (2000) Diet and the evolution of the earliest human ancestors. Proc Natl Acad Sci 97:13506–13511 Tebruegge M, Pantazidou A, Curtis N (2011) What’s bugging you? An update on the treatment of head lice infestation. Arch Dis Child Educ Pract Ed 96:2–8 Thalmann O, Fischer A, Lankester F, Pääbo S, Vigilant L (2007) The complex evolutionary history of gorillas: Insights from genomic data. Mol Biol Evol 24:146–158 186 J.M. Allen et al. Toups MA, Kitchen A, Light JE, Reed DL (2011) Origin of clothing lice indicates early clothing use by anatomically modern humans in Africa. Mol Biol Evol 28(1):29–32 Ubelaker JE, Payne E, Allison VF, Moore DV (1973) Scanning electron microscopy of the human pubic louse, Pthirus pubis (Linnaeus, 1758). J Parasitol 59(5):913–919 Ungar P (2004) Dental topography and diets of Australopithecus afarensis and early Homo. J Hum Evol 46:605–622 Ungar PS, Scott RS, Grine FE, Teaford MF (2010) Molar microwear textures and the diets of Australopithecus anamensis and Australopithecus afarensis. Proc Roy Soc Lond B Biol 365:3345–3354 Verhaegen M, Puech P-F, Munro S (2002) Aquarboreal ancestors? Trends Ecol Evol 17:212–217 Waldeyer L (1900) Ein Fall von Phthirius pubis im Bereiche des behaarten Kopfes. ChariteAnnalen, Berlin, XXV:494–499 Wheeler PE (1992) The influence of the loss of functional body hair on the water budgets of early hominids. J Hum Evol 23:379–388 White T (2003) Early hominids–diversity or distortion? Science 299:1994–1997 Whiteman NK, Parker PG (2005) Using parasites to infer host population history: a new rationale for parasite conservation. Anim Cons 8:175–181 Wilkinson RD, Steiper ME, Soligo C, Martin RD, Yang ZH, Tavare S (2011) Dating primate divergences through an integrated analysis of palaeontological and molecular data. Syst Biol 60(1):16–32 WoldeGabriel G, White TD, Suwa G, Renne P, de Heinzelin J, Hart WK, Heiken G (1994) Ecological and temporal placement of early Pliocene hominids at Aramis, Ethiopia. Nature 371:330–333 WoldeGabriel G, Ambrose SH, Barboni D, Bonnefille R, Bremond L, Currie B, DeGusta D, Hart WK, Murray AM, Renne PR, Jolly-Saad MC, Stewart KM, White TD (2009) The geological, isotopical, botanical, invertebrate and lower vertebrate surroundings of Ardipithecus ramidus. Science 326(5949):65e1–65e5 Wolfe ND, Dunavan CP, Diamond J (2007) Origins of major human infectious diseases. Nature 447(17):279–283 Yamagiwa J, Basabose AK (2006) Effects of fruit scarcity on foraging strategies of sympatric gorillas and chimpanzees. In: Hohmann G, Robbins M, Boesch C (eds) Feeding ecology in apes and other primates. Cambridge University Press, Cambridge, pp 73–96 Yamagiwa J, Maruhashi T, Yumoto T, Mwanza N (1996) Dietary and ranging overlap in sympatric gorillas and chimpanzees in Kahuzi-Biega National Park, Zaire. In: McGrew WC, Marchant LF, Nishida T (eds) Great ape societies. Cambridge University Press, Cambridge, pp 82–98 Yotova V, Lefebvre JF, Moreau C, Gbeha E, Hovhannesyan K, Bourgeois S, Bédarida S, Azevedo L, Amorim A, Sarkisian T, Avogbe P, Chabi N, Dicko MH, Amouzou ESKS, Sanni A, RobertsThomson J, Boettcher B, Scott RJ, Labuda D (2011) An X-linked haplotype of Neanderthal origin is present among all non-African populations. Mol Biol Evol 28(7):1957–1962