The Impact of Ecology, Demography, and Genetics on Primate Pelage
Open AccessWhat forces generate and maintain phenotypic diversity? This remains a central question in evolutionary biology and marks a main tenet of human biology. However, the topic can be difficult to study because phenotypes can be hard to quantify, shifts in phenotypic traits may be the result of solely neutral forces, and the proximate mechanisms underlying phenotypic variation are often not well characterized. Pelage (i.e., hair/fur), however, is an excellent trait to study the ultimate and proximate mechanisms influencing patterns of variation. Aspects of hair morphology are readily quantifiable with photography and microscopy, and hair phenotypes are genetically characterized (mainly due to research on laboratory or domestic animals). Changes in hair are often also shaped by natural and sexual selection, since it provides camouflage, protection, thermoregulatory, and signaling benefits (Allen et al., 2014; Hoekstra et al., 2005; Jones et al., 2018; Paus & Foitzik, 2004). Arguably hair (or the lack of it) is a trait that has contributed to the success of terrestrial mammals—including humans (Maderson, 2003). In this dissertation, I consider how ecology, demography, and genetics broadly contribute to the evolution of primate hair diversity.Of all mammals, primates have the most spectacular diversity in hair traits (i.e., long mustaches, greying, stripes, long capes). However, the forces generating this diversity are poorly understood. Most of what we know about what drives primate hair evolution has come from studies utilizing images of zoo-based animals or online stock photos—focused on only one or two body parts (Allen et al., 2014; Rakotonirina, Kappeler, & Fichtel, 2017; Santana et al., 2012; 2013). From these studies it is hypothesized that primate hair aids mostly in communication and crypsis. There is also a widely held assumption that hair color changes in non-human primates may signal age-related changes (as in humans). Yet, these hypotheses and assumptions remain mostly untested in wild or other natural populations. Furthermore, evidence about what genetic mechanisms underscore hair diversity remain largely inconclusive (Bradley et al., 2013). It is possible that patterns observed in the wild may bring forward stronger hypotheses to what genetic mechanisms drive primate hair variation. In Chapter 1, I review the cellular pathways of hair keratinization and melanogenesis and highlight key genes worthy of future study. I review what we know about primate hair biology, and touch on the promise of population genomics for uncovering the genetic basis of pigmentation and hair growth in non-human primates. I explain that hair is incredibly malleable and susceptible to rapid changes in the environment; and traits such as hair density may track environmental changes well. Based on what we know in systems such as rodents and quail, I hypothesize about the cellular and genomic underpinnings of primate pattern development, which begins during embryogenesis. I suggest a full understanding of primate hair biology will require comparative analysis (and functional tests) across model vertebrate taxa. However, I make a point to show that genetic mechanisms underlying hair variation seem distinct between wild and laboratory rodents—and are certainly distinct between humans and rodents (Ito & Wakamatsu, 2011; Suzuki et al., 1997). Thus, wild non-human primates remain an important (but understudied) comparator to understand hair evolution. In Chapter 2, I test if patterns of overall coloration within one wild population of diademed sifakas (Propithecus diadema)—containing highly variable hair phenotypes—are associated with ecology and/or demography. I use a semi quantitative approach to study hair color, in combination with ecological analyses. Using ecological-niche modeling (ENM), I find a climate gradient in temperature and precipitation in the forest—where the eastern forest block is typified by warmer temperatures and higher precipitation. The relationship indicates that dark sifakas are more likely to occur in colder regions that experience less rain. These results are the first evidence for Bogert’s rule in mammals, which suggests animals are darker in colder regions potentially due to thermoregulation. I also found there is a statistically significant association between facial complexity and contrast with climate, and that more complex faces are found in warmer and wetter (i.e., denser) forests. Thus, it is possible that complex faces may aid in individual identification in dense forests where signal visibility is lower. An alternative, but equally likely explanation, is that these patterns are merely the result of isolation by distance. For example, genetic drift may also be driving the divergence in facial pattern complexity—especially since lemurs are known to have high phylogenetic signal on facial color patterns. Clearly, robust population genomics in the region will help clarify to what extent neutral and non-neutral forces underlie color variation. However, a macro-scale analysis across the species or entire family may best contextualize these results. In Chapter 3, I test whether variation in pelage coloration and density across a highly variable clade of lemurs, containing the Propithecus genus (Indriidae family), is associated with climate, phylogeny, or opsin genotypes (the genetic basis of color vision). I collect phenotype data from both museum and living specimens with wild origins, and opsin genotypes sre derived from a subset of wild individuals. Many Indriidae populations exhibit polymorphic trichromacy, where only some females are trichromats (Jacobs et al., 2017). I find red hues in diurnal genera are associated with larger ranges in spectral sensitivity. It is possible that red hair aids with signaling across polymorphic trichromatic populations. I also find that climate is associated with hair color and density patterns across species. Darker coat colors are most likely to occur in warmer and denser forests for most of the clade, in line with Gloger’s rule (Gloger, 1833). However, surprisingly, dark coats are likelier to occur in colder forests across P. diadema—which is in line with results from Chapter 2. This latter result suggests distinct selective pressures acting on P. diadema pelage that warrants further detailed study. I also find evidence that Indriids with denser coats also co-occur in colder forests, and individuals with less hair live in open and hotter environments. The results expand and fortify previous hypotheses about early hominin hair evolution. Specifically, this serves as rare evidence for the body cooling hypothesis (Wheeler, 1992). I argue that hair coloration and growth phenotypes may have varied with ecology in early hominin evolution. Instead of becoming a “naked ape” in one-fell swoop, hominins likely gradually lost hair as the environmental conditions allowed. These results raise questions about convergent phenotypes between non-human primates and modern humans. In Chapter 4, I use photographs collected across three wild populations of chimpanzees (Pan troglodytes), to test if patterns of hair greying increase with age—as they do in modern humans. I score photos collected from three natural populations of chimpanzees—two wild and one captive. I find that, unlike the patterns seen in humans (Panhard et al., 2012), hair greying is not a salient marker of age in chimpanzees (Tapanes et al., 2020). While chimpanzee hair greying increases till approximately mid-life, it plateaus into old age. Additionally, I find the propensity to grey is distinct across wild and captive chimpanzees. Specifically, captive chimpanzees are likely to grey earlier than their wild counterparts and score overall higher marks for “grey hair” phenotypes. This may indicate the proximate mechanism behind greying is tied to stress, disease, or greater exposure to UV radiation (Zhang et al., 2020). These results also act as evidence that phenotypic changes documented in captive populations may not follow phenotypic trends in wild populations. Lastly, I hypothesize progressive greying as a marker of age likely originated after the Pan-human split, and selection potentially acts to maintain heavy eumelanin coat colors in some non-human species (Tapanes et al., 2020). In Chapter 5, I summarize the findings of the previous chapters and provide additional preliminary evidence gathered on the evolution of primate hair. This chapter provides supplemental elements for Chapters 1, 3 and 4 – that is, information/data that did not fit within the manuscript confines of the individual chapters but was important to document in the dissertation, nonetheless. As a supplement to Chapter 1, I show that primates express MITF (the master melanocyte regulator) in both pigmented and un-pigmented tufts of hair. This suggests white hair patches in primates contain melanocytes and shows a dissimilar pattern from laboratory rodents and domesticated animals (e.g., cats, dogs). The pattern, instead, is similar to mechanisms documented in wild rodents (Haupaix & Manceau, 2019; Manceau et al., 2010). This is an important finding because most of the hypotheses guiding what genes and pathways govern primate hair phenotypes originate on studies in laboratory and domesticated animals. As a supplement to Chapter 3, I showed that hair density and coloration are largely uncorrelated and decoupled processes. The crown is the only body region across Indriidae where there is a moderate and statistically significant correlation between density and coloration. I hypothesize this may have a thermoregulatory benefit given Indriids are vertical clingers and leapers but this requires further study. As a supplement to Chapter 4, I show that chimpanzee hair greying and facial color changes are weakly but significantly correlated—but that facial skin color changes also fail to indicate age. Thus, the melanogenesis pathways of skin and hair pigmentation may be linked. Chimpanzees are also like other wild mammals in the fact that skin color can only be used to age chimpanzees broadly (i.e., younger, middle-aged, older) (Read et al., 2018; McConkey et al., 2002). This is in contrast to most human populations, where skin becomes paler and thinner with age. Interestingly, I find sex-class differences in skin pigmentation in wild populations—but not in the captive population. Wild female chimpanzees are more likely to have darker faces, and this could be explained by a difference in hormones, life history, or environmental exposures. Importantly, taken together, these results highlight that the evolution of non-human primate hair is more nuanced and population-specific than previously appreciated. While laboratory models may help establish the functional consequences of primate hair phenotypes (as suggested in Chapter 1), they are likely a poor evolutionary model for how and why primate hair varies in nature. In conclusion, I argue that hair is a great trait by which we can understand the evolution of phenotypic diversity, but it is not a “simple” trait. Non-human primate hair is potentially a complex trait—similar to human skin and hair variation (which are population-specific, under pleiotropic control, and shaped by local selective pressures) (Quillen et al., 2019). Similarly, a variety of processes and genes likely contribute to hair growth properties in wild nonhuman primates—unlike what is seen during artificial selection of hair traits in animal breeding. The key to understanding primate hair evolution will be research on wild populations, using carful phenotyping, climate analyses, population genomics, selection analyses across many genes, and gene expression studies. For primates (including humans), it is likely a combination of selective and neutral forces (such as population size, gene flow, etc.) which impact hair variation evolution within and across populations in nuanced population-specific ways.
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