The naked ape as an evolutionary model, 50 years later

Summary Variation in the strength of age‐dependent natural selection shapes differences in ageing rates across species and populations. Likewise, sexual selection can promote divergent patterns of senescence across the sexes. However, the effects of these processes on the evolution of ageing have largely been considered independently, and interactions between them are poorly understood. We use experimental evolution to investigate how natural and sexual selection affect life span and ageing in Drosophila simulans. Replicate populations were evolved under lifetime monogamy (relaxed sexual selection) or lifetime polyandry (elevated sexual selection) and at one of two temperatures, 25 °C (relaxed natural selection) or 27 °C (enhanced natural selection), in a fully factorial design. We measured longevity in 150 individually housed flies taken from each of three replicate populations per selection regime. We found that natural and sexual selection affected the evolution of life span via sex‐specific effects on different ageing parameters (ageing rate vs. baseline mortality): natural selection reduced the rate of ageing in both sexes but increased male baseline mortality, while sexual selection elevated baseline mortality in both sexes but particularly in males. This means that sexual and natural selection interacted to reduce male life span but acted on female life span by independently affecting particular ageing parameters. Sex‐specific effects of sexual and natural selection may help explain the diverse patterns of ageing seen in nature but complicate predictions about how ageing and life span evolve across the sexes

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.

Male túngara frogs appear in choruses and have well-defined vocal cords at a size of 19 mm snout-vent length (SVL), but they do not begin producing advertisement calls until they reach approximately 24 mm SVL. Is this because the larynx is not fully mature until the latter point, or is it because the calls of small-bodied adults would not be attractive enough to outweigh the costs (energy, predation and parasitism) of producing them? We investigate this question by tuning bond graph models of the túngara frog larynx with parameter values across this critical body size range. Simulations were informed by a new set of diceCT-based measurements of key laryngeal morphological features from an ontogenetic series. Models produce sustained oscillations in airflow through the larynx (sound) with species-typical spectral features across the full range of the ontogenetic ‘silent zone’, suggesting that muteness during this period is facultative and not physically enforced. This result illuminates the morphological and behavioural consequences of an interplay of natural and sexual selection. Sexual selection and developmental constraints may lead the early development of laryngeal vibratory tissues, while natural selection (energetic costs and predation avoidance) and sexual selection (reduced call attractiveness) act to mute smaller adult frogs.

Darwin, Charles (Darwinism)

The relative numbers of trunk (body) and caudal (tail) vertebrae in snakes might be influenced by at least four processes: (1) natural selection for crawling speed, (2) fecundity selection for larger trunk size in females, (3) sexual selection for longer bodies or tails in males and/or (4) developmental constraints (if an increase in the number of body vertebrae requires a decrease in the number of tail vertebrae, or vice versa). These four hypotheses generate different predictions about the relationship between sex differences in the numbers of body vertebrae vs. tail vertebrae. I collated published data to test these predictions, both with raw data and using phylogenetically independent contrasts. Some snake lineages show a negative correlation between the magnitude of sex disparities in trunk vs. caudal vertebrae whereas other lineages show the reverse pattern, or no correlation. Thus, different selective pressures seem to have been important in different lineages. Vertebral numbers in snakes may offer a useful model system in which to explore the conflicts between natural, fecundity and sexual selection.

The study of the human skin evolution, allows a new vision to ancient questions such as the significance of human skin color variation, the correlations between bipedality and loss of body hair, and the correlations among epidermal appendages and structures of the skin with the changes on environment and evolution of humans. Paleodermatology would be an appropriated term to designate the study of the human skin evolution. The etymology of this word comes from a Greek root (paleo = ancient). It is a multidisciplinary subject for researchers such as dermatologists, anthropologists, physiologists, and orthopedics. It should include the evaluations regarding physiology, thermoregulation, and the evolution of the human skin structures.

Concurrent natural and sexual selection have been inferred from laboratory and comparative studies in a number of taxa, but are rarely measured in natural populations. Because the interaction of these two general categories of selection may be complex when they occur simultaneously, empirical evidence from natural populations would help us to understand this interaction and probably give us greater insight into each separate episode as well. In male sockeye salmon, sexual selection for larger body size has been indicated in both deep and shallow water habitats. However, in shallow habitats male sockeye are generally smaller and less deep-bodied than in deep habitats, a difference that has been ascribed to natural selection. We measured concurrent natural and sexual selection in two years on breeding male sockeye salmon with respect to body size, body shape, and time of arrival to the breeding grounds. Natural selection was variable in effect and sexual selection was variable in intensity in these two years. The patterns of selection also appear to be interdependent; areas where predation on spawning adults is not intense have yielded different patterns of sexual selection than those measured here. It appears that some of the body shape differences in sockeye salmon associated with different spawning habitats, which were previously attributed to selective mortality, may be a result of different patterns of sexual selection in the different habitats. Total selection resulting from the combination of both natural and sexual selection was less intense than either natural or sexual selection in most cases. Measurement of concurrent selection episodes in nature may help us to understand whether the pattern of differential sexual selection is common, and whether observed patterns of habitat-related differentiation may be due to differences in sexual selection.

The importance of sexual selection in population divergence is of much interest, mainly because it is thought to cause reproductive isolation and hence could lead to speciation. Sexually selected traits have been hypothesized to diverge faster between populations than other traits, presumably because of differences in the strength, mechanism or dynamics of selection. We investigated this by quantifying population divergence in eight morphological characters in 12 south Swedish populations of a sexually dimorphic damselfly, the banded demoiselle (Calopteryx splendens). The morphological characters included a secondary sexual character, the male melanized wing spot, which has an important function in both inter- and intrasexual selection. In addition, we investigated molecular population divergence, revealed by amplified fragment length polymorphism (AFLP) analysis. Molecular population divergence was highly significant among these Northern European populations (overall F(st)=0.054; pairwise population F(st)'s ranged from approximately 0 to 0.13). We found evidence for isolation-by-distance (r=0.70) for the molecular markers and a significant correlation between molecular and phenotypic population divergence (r=0.39). One interpretation is that population divergence for the AFLP loci are affected by genetic drift, but is also indirectly influenced by selection, due to linkage with loci for the phenotypic traits. Field estimates of sexual and natural selection from two of the populations revealed fairly strong sexual selection on wing spot length, indicating that this trait has the potential to rapidly diverge, provided that variation is heritable and the observed selection is chronic.

Understanding the evolutionary causes of phenotypic variation among populations has long been a central theme in evolutionary biology. Several factors can influence phenotypic divergence, including geographic isolation, genetic drift, divergent natural or sexual selection, and phenotypic plasticity. But the relative importance of these factors in generating phenotypic divergence in nature is still a tantalizing and unresolved problem in evolutionary biology. The origin and maintenance of phenotypic divergence is also at the root of many ongoing debates in evolutionary biology, such as the extent to which gene flow constrains adaptive divergence (Garant et al. 2007) and the relative importance of genetic drift, natural selection, and sexual selection in initiating reproductive isolation and speciation (Coyne & Orr 2004). In this issue, Wang & Summers (2010) test the causes of one of the most fantastic examples of phenotypic divergence in nature: colour pattern divergence among populations of the strawberry poison frog (Dendrobates pumilio) in Panama and Costa Rica (Fig. 1). This study provides a beautiful example of the use of the emerging field of landscape genetics to differentiate among hypotheses for phenotypic divergence. Using landscape genetic analyses, Wang & Summers were able to reject the hypotheses that colour pattern divergence is due to isolation-by-distance (IBD) or landscape resistance. Instead, the hypothesis left standing is that colour divergence is due to divergent selection, in turn driving reproductive isolation among populations with different colour morphs. More generally, this study provides a wonderful example of how the emerging field of landscape genetics, which has primarily been applied to questions in conservation and ecology, now plays an essential role in evolutionary research.

Both natural and sexual selection can shape sexual dimorphism. However, determination of the contribution of these selection pressures is challenging. In lizards, sexual selection can contribute to the larger head size of males than that of females. However, males and females can also diverge in their head size to prey on different food resources under conditions of limited resources (and/or high competitors). Here, 109 individuals from two sympatric desert racerunners (Eremias grammica: 28 males and 30 females; Eremias velox: 25 males and 26 females) were studied to determine their sexual head shape (head length, width, and depth). Additionally, 191 and 169 feces samples of E. grammica and E. velox, respectively, were collected to assess the niche divergence hypothesis (a proxy for natural selection). We found that both species had dimorphic head shapes; male heads (i.e., length, width, and depth) were significantly larger than female heads (P < 0.05, in all cases) in E. grammica, and male heads of E. velox were significantly longer than those of females (P < 0.05). Chi-square test revealed that there were significant differences in the proportion (Hymenopteran and Orthopteran) and sizes of prey type between the two sexes of E. grammica; conspecific males and females of E. velox differed in the proportion of Coleopteran and Hymenopteran prey. Both males and females of these two species had a high niche overlap index (range from ∼ 0.78 to 0.99) with each other. There were also significant differences in the sizes of the heads and prey between the two species (P < 0.05). However, the interspecific differences were mainly caused by interspecific male–male differences in morphological and prey traits. In summary, we believe that both natural (pressures from resource competition) and sexual selection drive sexual head shape dimorphism in these two sympatric lizards, owing to high food resource competition in arid regions. Therefore, head trait divergence can reduce competition by resulting in a preference for different prey types.

Natural and sexual selection shape the evolution of species but the interplay between them is poorly understood. Two phylogenetic studies on birds have suggested that species with greater sexual dichromatism have a broader habitat use. We show that in agamid lizards, species with more elaborate secondary sexual traits are also ecologically more opportunistic. Species with greater dimorphism in head size and ornamentation have greater altitudinal range and broader habitat use, respectively, and species with greater sexual dichromatism have wider microhabitat use. Body size was positively associated with sexual and ecological generalism, but associations between ecological and sexual traits remained after accounting for body size. We suggest that sexual and natural selection may be linked either because sexual selection can promote generalism at the population level by favouring 'good genes', or because higher population densities may be associated with both stronger sexual selection and broader resource use.

Treating color patterns in a geometric morphometrics framework reveals rapid rates of color evolution that are explained by a combination of intrinsic organismal features (color variation among patches) and geography within a cosmopolitan radiation of birds.

As the fifth and supposedly ‘naked ape’, modern humans do not possess an all-encompassing, thick and pigmented pelage, other than in utero. Selection for shorter and finer (vellus) hair has resulted in scalp hair being the only hair remaining visible in any significant quantity. These specialized, so-called terminal hairs are capable of growing to a greater length than on any other mammal. In an age seemingly obsessed with celebrity and fashion, abundant hair on the female scalp has become an almost mandatory signal of youth, health and femininity. For that reason, a massive global industry has developed, which is exclusively devoted to its care and management. However, with the remorseless march of time, this glorious display may diminish in density and volume, resulting both in practical grooming and also psychological issues. The loss of density is now recognized as a genuine and quantifiable problem, but understanding where normal age-related loss ends, and disease begins, remains a conundrum for the physician. When current diagnostic criteria do not match their self-assessment, patients often feel frustrated and neglected and can resort to unsupported therapies. Terminal hairs are not completely confined to the scalp. While the onset of menarche leads to the development of terminal hairs in the expected secondary sexual areas (most notably axillae and genital areas), it can also lead to the development of terminal hairs in other areas such as the face and body. In many cultures, any extraneous terminal hair growth, and even growth in the secondary sexual areas, is regarded not only as undesirable but as personally and socially intolerable. For that reason, millions of women seek pharmacy, beautician or medical advice on this matter; however, they face a plethora of different options and many unsubstantiated regimens. Many more women are denied by economic circumstances from the more advanced therapies available in industrialized nations. Unlike conventional Hair Symposia, this Procter & Gamble sponsored meeting provided a forum for a world class faculty of dermatologists and scientists, who presented their diverse perspectives in all aspects of female scalp, facial and body hair issues. These proceedings summarize the oral presentations given at this symposium, and bring a number of new insights into the lifetime of the female hair cycle and the role that sex hormones (androgens and oestrogens) play in common female hair loss disorders. Comprehensive reviews of the criteria for intervention in female pattern hair loss will be of inestimable help to practising dermatologists in deciding on the best available treatment options. The practical aspects of managing extraneous facial and body hair, including an evidence-based assessment of office and home laser devices is presented, bringing a new level of clarity to this evolving field. An update of the latest research from Procter & Gamble scientists offers insights into the technologies behind the next generation of cosmetic hair care and hair management products and their place in the dermatologist’s armamentarium. To the casual observer, research in this field of hair may appear to have stagnated in recent years. However, as Mark Twain remarked, ‘reports of my death may be exaggerated’. This publication illustrates that in the 4 years since the last World Congress of Dermatology the field is very much alive, with the collaboration of some of the world’s leading dermatologists and industry scientists bringing benefits to millions of women around the world. Financial support for publication of this supplement was provided by Procter & Gamble. J. G. is a medical consultant for Procter & Gamble.

New genes (or young genes) are structural novelties pivotal in mammalian evolution. Their phenotypic impact on humans, however, remains elusive due to the technical and ethical complexities in functional studies. Through combining gene age dating with Mendelian disease phenotyping, our research reveals that new genes associated with disease phenotypes steadily integrate into the human genome at a rate of ~ 0.07% every million years over macroevolutionary timescales. Despite this stable pace, we observe distinct patterns in phenotypic enrichment, pleiotropy, and selective pressures between young and old genes. Notably, young genes show significant enrichment in the male reproductive system, indicating strong sexual selection. Young genes also exhibit functions in tissues and systems potentially linked to human phenotypic innovations, such as increased brain size, bipedal locomotion, and color vision. Our findings further reveal increasing levels of pleiotropy over evolutionary time, which accompanies stronger selective constraints. We propose a “pleiotropy-barrier” model that delineates different potentials for phenotypic innovation between young and older genes subject to natural selection. Our study demonstrates that evolutionary new genes are critical in influencing human reproductive evolution and adaptive phenotypic innovations driven by sexual and natural selection, with low pleiotropy as a selective advantage.

The evolutionary dynamics of color pattern diversification in animals is strongly influenced by visual interactions within and among species. While much attention has been given to color pattern variation in the human-visible range, perception outside this range is observed in a wide array of species and is poised to influence color pattern evolution. Butterfly species often show sensitivity to ultraviolet (UV) light, impacting wing color pattern diversification as their evolution is influenced by both predator vision and sexual selection. Here, we explore UV color pattern diversification in Papilionidae within a comparative phylogenetic framework by quantifying variation from UV photographs of museum specimens using a machine-learning-based method. We find decoupled dorsal and ventral UV color pattern evolution, with brighter and more rapidly evolving ventral sides, especially in males. Conversely, we find a smaller dorso-ventral difference in visible-light color patterns. Moreover, we find divergence in male ventral UV patterns in closely related sympatric species, even after accounting for variation due to visible-light patterns. These results suggest an influence of sexual selection on UV ventral pattern diversification. These findings highlight how the trade-off between sexual and natural selection may lead to contrasted evolution of ventral vs. dorsal sides of the same organ.