Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression

Body size may be an important factor influencing the evolution of facial expression in anthropoid primates due to allometric constraints on the perception of facial movements. Given this hypothesis, I tested the prediction that observed facial mobility is positively correlated with body size in a comparative sample of nonhuman anthropoids. Facial mobility, or the variety of facial movements a species can produce, was estimated using a novel application of the Facial Action Coding System (FACS). I used FACS to estimate facial mobility in 12 nonhuman anthropoid species, based on video recordings of facial activity in zoo animals. Body mass data were taken from the literature. I used phylogenetic generalized least squares (PGLS) to perform a multiple regression analysis with facial mobility as the dependent variable and two independent variables: log body mass and dummy-coded infraorder. Together, body mass and infraorder explain 92% of the variance in facial mobility. However, the partial effect of body mass is much stronger than for infraorder. The results of my study suggest that allometry is an important constraint on the evolution of facial mobility, which may limit the complexity of facial expression in smaller species. More work is needed to clarify the perceptual bases of this allometric pattern.     

Plain faces are more expressive: comparative study of facial colour,mobility and musculature in primates

Facial colour patterns and facial expressions are among the most important phenotypic traits that primates use during social interactions. While colour patterns provide information about the sender''s identity, expressions can communicate its behavioural intentions. Extrinsic factors, including social group size, have shaped the evolution of facial coloration and mobility, but intrinsic relationships and trade-offs likely operate in their evolution as well. We hypothesize that complex facial colour patterning could reduce how salient facial expressions appear to a receiver, and thus species with highly expressive faces would have evolved uniformly coloured faces. We test this hypothesis through a phylogenetic comparative study, and explore the underlying morphological factors of facial mobility. Supporting our hypothesis, we find that species with highly expressive faces have plain facial colour patterns. The number of facial muscles does not predict facial mobility; instead, species that are larger and have a larger facial nucleus have more expressive faces. This highlights a potential trade-off between facial mobility and colour patterning in primates and reveals complex relationships between facial features during primate evolution.     

Sexual selection,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Habitat use affects morphological diversification in dragon lizards

Habitat use may lead to variation in diversity among evolutionary lineages because habitats differ in the variety of ways they allow for species to make a living. Here, we show that structural habitats contribute to differential diversification of limb and body form in dragon lizards (Agamidae). Based on phylogenetic analysis and ancestral state reconstructions for 90 species, we find that multiple lineages have independently adopted each of four habitat use types: rock‐dwelling, terrestriality, semi‐arboreality and arboreality. Given these reconstructions, we fit models of evolution to species’ morphological trait values and find that rock‐dwelling and arboreality limit diversification relative to terrestriality and semi‐arboreality. Models preferred by Akaike information criterion infer slower rates of size and shape evolution in lineages inferred to occupy rocks and trees, and model‐averaged rate estimates are slowest for these habitat types. These results suggest that ground‐dwelling facilitates ecomorphological differentiation and that use of trees or rocks impedes diversification.     

Arboreality and the evolution of disease resistance in ants

1. Parasites are an important selective force for almost all organisms and drive the evolution by hosts of defence mechanisms that are energetically costly. The strength of parasitism will vary between host species according to their specific ecology and life history, and so the optimal investment in costly resistance mechanisms is also likely to vary between host species with differing ecologies. 2. Parasites are particularly important for social species such as ants, but very little is known about the strength of selection in different species. It has been suggested that, because arboreality reduces exposure to soil‐borne fungal pathogens, arboreal ant species may invest less in disease resistance. However, testing hypotheses such as this requires data on disease resistance in multiple species, and such studies have not previously been attempted. 3. Here we examine the arboreality hypothesis by comparing the disease resistance of seven Neotropical ant species with different degrees of arboreality. We exposed ants to controlled doses of the generalist, virulent fungal parasite, Metarhizium anisopliae (Metchnikoff) Sorokin. We then monitored survival, parasite sporulation, and the anti‐fungal grooming response of the ants. 4. Contrary to the hypothesis, we found that arboreal species were not less resistant to M. anisopliae than species that were ground‐dwelling, and that the species that inhabited both arboreal and ground habitats had the greatest resistance. Surprisingly, the most resistant species was one that lacked the antibiotic‐producing metapleural gland, previously considered the lynchpin of disease resistance in ants. 5. The results suggest that it may be the diversity of parasites encountered that is the greatest selection pressure. Further experimental studies with other parasites are needed to confirm the generality of the results, and similar comparative studies of other taxa are needed to understand the relationship between host ecology and the evolution of disease resistance.     

Understanding hind limb weight support in chimpanzees with implications for the evolution of primate locomotion

Most quadrupedal mammals support a larger amount of body weight on their forelimbs compared with their hind limbs during locomotion, whereas most primates support more of their body weight on their hind limbs. Increased hind limb weight support is generally interpreted as an adaptation that reduces stress on primates' highly mobile forelimb joints. Thus, increased hind limb weight support was likely vital for the evolution of primate arboreality. Despite its evolutionary importance, the mechanism used by primates to achieve this important kinetic pattern remains unclear. Here, we examine weight support patterns in a sample of chimpanzees (Pan troglodytes) to test the hypothesis that limb position, combined with whole body center of mass position (COM), explains increased hind limb weight support in this taxon. Chimpanzees have a COM midway between their shoulders and hips and walk with a relatively protracted hind limb and a relatively vertical forelimb, averaged over a step. Thus, the limb kinematics of chimpanzees brings their feet closer to the COM than their hands, generating greater hind limb weight support. Comparative data suggest that these same factors likely explain weight support patterns for a broader sample of primates. It remains unclear whether primates use these limb kinematics to increase hind limb weight support, or whether they are byproducts of other gait characteristics. The latter hypothesis raises the intriguing possibility that primate weight support patterns actually evolved as byproducts of other traits, or spandrels, rather than as adaptations to increase forelimb mobility. Am J Phys Anthropol, 2009. © 2008 Wiley‐Liss, Inc.     

Size dependency in colour patterns of Western Palearctic carabids

Body colouration is of high evolutionary relevance for most animals. Several competing hypotheses exist regarding the evolutionary reasons for animal colouration ranging from predator avoidance and sexual advertisement to neutral selection. Among these hypotheses, biophysical principles suggest the thermoregulatory importance of dark colouration which in turn strongly depends on species body size. This body size – darkness trade‐off is based on sound theoretical background conceptualized in the thermal melanism hypothesis and is confirmed by numerous case studies for individual species. However, evidence for the general relevance of this trade‐off on large spatial and taxonomic scale is still missing. Here we specifically focus on this body size – colouration trade‐off for a hyper‐diverse and cosmopolitan group of insects, namely ground beetles. We combined colour information with trait data and distributional as well as bioclimatic attributes for more than 1000 carabid species from the entire Western Palearctic. We quantified species‐specific body colouration from high‐quality, standardised digital photographs using the Munsell colour system. We detect a strong increase of colour darkness with body size from small to medium‐sized carabids up to a body size threshold of 15 mm which is consistent with the thermal melanism hypothesis. However, body size showed no effect above this threshold and colour darkness remained constantly high which is in accordance with previous ideas about the size‐dependency of thermoregulative control mechanisms (size dependence hypothesis). By demonstrating a strong tendency towards darkness with increasing body size, we illustrate the inter‐specific relevance of body colouration for this cosmopolitan group of ectotherms on a continental scale. The putative thermoregulative trade‐off between body size and melanism seems to be of significant importance for carabids on a broad spatial scale and may be a general but still underestimated phenomenon for ectotherms in general, although other mechanistic drivers cannot be completely neglected.     

THE VARIABILITY IS IN THE SEX CHROMOSOMES

Sex differences in the mean trait expression are well documented, not only for traits that are directly associated with reproduction. Less is known about how the variability of traits differs between males and females. In species with sex chromosomes and dosage compensation, the heterogametic sex is expected to show larger trait variability (“sex‐chromosome hypothesis”), yet this central prediction, based on fundamental genetic principles, has never been evaluated in detail. Here we show that in species with heterogametic males, male variability in body size is significantly larger than in females, whereas the opposite can be shown for species with heterogametic females. These results support the prediction of the sex‐chromosome hypothesis that individuals of the heterogametic sex should be more variable. We argue that the pattern demonstrated here for sex‐specific body size variability is likely to apply to any trait and needs to be considered when testing predictions about sex‐specific variability and sexual selection.     

Consistent size‐independent harvest selection on fish body shape in two recreationally exploited marine species

Harvesting wild animals may exert size‐independent selection pressures on a range of morphological, life history, and behavioral traits. Most work so far has focused on selection pressures on life history traits and body size as morphological trait. We studied here how recreational fishing selects for morphological traits related to body shape, which may correlate with underlying swimming behavior. Using landmark‐based geometric morphometrics, we found consistent recreational fishing‐induced selection pressures on body shape in two recreationally exploited marine fish species. We show that individuals with larger‐sized mouths and more streamlined and elongated bodies were more vulnerable to passively operated hook‐and‐line fishing independent of the individual's body size or condition. While the greater vulnerability of individuals with larger mouth gapes can be explained by the direct physical interaction with hooks, selection against streamlined and elongated individuals could either involve a specific foraging mode or relate to underlying elevated swimming behavior. Harvesting using passive gear is common around the globe, and thus, size‐independent selection on body shape is expected to be widespread potentially leaving behind individuals with smaller oral gapes and more compact bodies. This might have repercussions for food webs by altering foraging and predation.     

Energy and interspecific body size patterns of amphibian faunas in Europe and North America: anurans follow Bergmann's rule, urodeles its converse

Aim To describe broad‐scale geographical patterns of body size for European and North American amphibian faunas and to explore possible processes underlying these patterns. Specifically, we propose a heat balance hypothesis, as both heat conservation and heat gain determine the heat balance of ectotherms, and test it along with five other hypotheses that have a possible influence on body size gradients: size dependence, migration ability, primary productivity, seasonality and water availability. Location Western Europe and North America north of Mexico. Methods We processed distribution maps for native amphibian species to estimate the mean body size in 110 × 110 km cells and calculated eight environmental predictors to explore the relationship between environmental gradients and the observed patterns. We used least squares regression modelling and model selection approaches based on information theory to evaluate the relative support for each hypothesis. Results We found consistent body size gradients and similar relationships to environmental variables within each amphibian group in Europe and North America. Annual potential evapotranspiration, a measure of environmental energy, was the strongest predictor of mean body size in both regions. However, the contrasting responses to ambient energy in each group resulted in opposite geographical patterns, i.e. anurans increased in size from high‐ to low‐energy areas in both continents and urodeles showed the opposite pattern. Main conclusions Our results support the heat balance hypothesis, suggesting that the thermoregulatory abilities of anurans would allow them to reach larger sizes in colder climates by optimizing the trade‐off between heating and cooling rates, whereas a lack of such strategies among urodele faunas would explain why these organisms tend to be smaller in cooler areas. These findings may also have implications for the role of climate warming on the global decline of amphibians.     

Grooming and group cohesion in primates: implications for the evolution of language

It is well established that allogrooming, which evolved for a hygienic function, has acquired an important derived social function in many primates. In particular, it has been postulated that grooming may play an essential role in group cohesion and that human language, as verbal grooming or gossip, evolved to maintain group cohesion in the hominin lineage with its unusually large group sizes. Here, we examine this group cohesion hypothesis and test it against the alternative grooming-need hypothesis which posits that rates of grooming are higher in species where grooming need (i.e. the motivation to groom for hygiene and its associated psychological reward) is more pronounced. This alternative predicts that the derived social function of grooming evolved mostly in those lineages that had the highest exposure to ectoparasites and dirt, i.e. terrestrial species. A detailed comparative analysis of 74 species of wild primates, controlling for phylogenetic non-independence, showed that terrestriality was a highly significant predictor of allogrooming time, consistent with the prediction. The predictions of the group cohesion hypothesis were not supported, however. Group size did not predict grooming time across primates, nor did it do so in separate intra-population analyses in 17 species. Thus, there is no comparative support for the group-cohesion function of allogrooming, which questions the role of grooming in the evolution of human language.     

Coevolution of Facial Expression and Social Tolerance in Macaques

The purpose of this study is to test the hypothesis that social tolerance drives the evolution of facial expression in macaques. Macaque species exhibit a range of social styles that reflect a continuum of social tolerance. Social interactions in more tolerant taxa tend to be less constrained by rank and kinship than in less‐tolerant macaques. I predicted that macaques that are more tolerant would exhibit a wider range of facial displays than less‐tolerant species because interactions that are open to negotiation are characterized by greater uncertainty than interactions that are constrained by rank or kinship. To test this hypothesis, I conducted a phylogenetically informed regression analysis (N = 11) using previously published data on repertoire size and two quantitative measures of social tolerance (conciliatory tendency and counter‐aggression). As predicted, macaques with more tolerant social styles tended to have larger repertoires than less‐tolerant species. These results support the hypothesis that increased social tolerance favors the elaboration of communication to mitigate uncertainty.     

Fruit–frugivore interactions in two southern hemisphere forests: allometry,phylogeny and body size

The size of fleshy fruits spans several orders of magnitude. However, the evolution of fruit size diversity is poorly understood. Fruit size diversity is hypothesised to result from several potential processes. The frugivore hypothesis postulates that different‐sized animal fruit consumers select for different‐sized fruits. The correlated selection hypothesis postulates that fruit size is allometrically related to other plant traits (e.g. leaf size, plant height); therefore differences in fruit size result from correlated evolution with other plant traits. We tested the frugivore and correlated selection hypotheses as potential explanations for fruit size diversity in two New Zealand study sites. We observed birds foraging for fruits over two fruiting seasons at each site and measured fruit size, leaf size and plant height in a total of 32 plant species. Relationships between average fruit size, leaf size, plant size and the average size of birds consuming each fruit species were then evaluated using phylogenetically independent contrasts. Similar results were obtained in both study sites. Fruit size was correlated with the size of avian fruit consumers, but was unrelated to leaf size or plant height. Therefore, results falsified the correlated selection hypothesis but failed to falsify the frugivore hypothesis. Although results suggest that frugivores may have influenced the evolution of fruit size in New Zealand, further study is needed to generate a mechanistic understanding of how frugivores may have selected for interspecific variation in fruit size.     

Niche divergence builds the case for ecological speciation in skinks of the Plestiodon skiltonianus species complex

Adaptation to different thermal environments has the potential to cause evolutionary changes that are sufficient to drive ecological speciation. Here, we examine whether climate‐based niche divergence in lizards of the Plestiodon skiltonianus species complex is consistent with the outcomes of such a process. Previous work on this group shows that a mechanical sexual barrier has evolved between species that differ mainly in body size and that the barrier may be a by‐product of selection for increased body size in lineages that have invaded xeric environments; however, baseline information on niche divergence among members of the group is lacking. We quantified the climatic niche using mechanistic physiological and correlative niche models and then estimated niche differences among species using ordination techniques and tests of niche overlap and equivalency. Our results show that the thermal niches of size‐divergent, reproductively isolated morphospecies are significantly differentiated and that precipitation may have been as important as temperature in causing increased shifts in body size in xeric habitats. While these findings alone do not demonstrate thermal adaptation or identify the cause of speciation, their integration with earlier genetic and behavioral studies provides a useful test of phenotype–environment associations that further support the case for ecological speciation in these lizards.     

SPEED AND STAMINA TRADE-OFF IN LACERTID LIZARDS

Abstract.— Morphological and physiological considerations suggest that sprinting ability and endurance capacity put conflicting demands on the design of an animal's locomotor apparatus and therefore cannot be maximized simultaneously. To test this hypothesis, we correlated size‐corrected maximal sprint speed and stamina of 12 species of lacertid lizards. Phylogenetically independent contrasts of sprint speed and stamina showed a significant negative relationship, giving support to the idea of an evolutionary trade‐off between the two performance measures. To test the hypothesis that the trade‐off is mediated by a conflict in morphological requirements, we correlated both performance traits with snout‐vent length, size‐corrected estimates of body mass and limb length, and relative hindlimb length (the residuals of the relationship between hind‐ and forelimb length). Fast‐running species had hindlimbs that were long compared to their forelimbs. None of the other size or shape variables showed a significant relationship with speed or endurance. We conclude that the evolution of sprint capacity may be constrained by the need for endurance capacity and vice versa, but the design conflict underlying this trade‐off has yet to be identified.     

Pitfalls in understanding the functional significance of genital allometry

The male genitalia of arthropods consistently show negative static allometry (the genitalia of small males of a species are disproportionally large, and those of large males are disproportionally small). We discuss relations between the ‘one‐size‐fits‐all’ hypothesis to explain this allometry and the regimes of selection that may be acting on genitalia. We focus on the contrasts between directional vs. stabilizing selection, and natural vs. sexual selection. In addition, we point out some common methodological problems in studies of genital allometry. One‐size‐fits‐all types of arguments for negative allometry imply net stabilizing selection, but the effects of stabilizing selection on allometry will be weaker when the correlation between body size and the trait size is weaker. One‐size‐fits‐all arguments can involve natural as well as sexual selection, and negative allometry can also result from directional selection. Several practical problems make direct tests of whether directional or stabilizing selection is acting difficult. One common methodological problem in previous studies has been concentration on absolute rather than relative values of the allometric slopes of genitalia; there are many reasons to doubt the usefulness of comparing absolute slopes with the usual reference value of 1.00. Another problem has been the failure to recognize that size and shape are independent traits of genitalia; rapid divergence in the shape of genitalia is thus not paradoxical with respect to the reduced variation in their sizes that is commonly associated with negative allometric scaling.     

Body size and extinction risk in Australian mammals: An information‐theoretic approach

The critical weight range (CWR) hypothesis for Australian mammals states that extinctions and declines have been concentrated in species with body mass between 35 g and 5.5 kg. The biological basis for this hypothesis is that species of intermediate size are disproportionately impacted by introduced predators. The CWR hypothesis has received support from several statistical studies over the past decade, although the evidence is weaker or non‐existent for certain groups such as mesic‐zone mammals and arboreal mammals. In this study, we employ an information‐theoretic model selection approach to gain further insights into the relationship between body mass and extinction risk in Australian mammals. We find evidence, consistent with the CWR hypothesis, that extinction risk peaks at intermediate body masses for marsupials, rodents and ground‐dwelling species, but not for arboreal species. In contrast to previous studies, we find that the CWR describes extinction patterns in the mesic zone as well as the arid zone. In the mesic zone, there is also a weaker tendency for large species above the CWR to be more vulnerable, consistent with extinction patterns on other continents. We find that a more biological plausible Gaussian distribution consistently fits the data better than the polynomial models that have been used in previous studies. Our results justify conservation programmes targeted at species within the CWR across Australia.     

Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size

Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade‐offs between brain size and sexual traits. Instead, larger‐brained males had higher expression of several primary and precopulatory sexual traits – they had longer genitalia, were more colourful and developed longer tails than smaller‐brained males. Larger‐brained males were also in better body condition when housed in single‐sex groups. There was no difference in post‐copulatory sexual traits between males from the large‐ and small‐brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.     

Arboreallty and morphological evolution in ground beetles (Carabidae: Harpalinae): testing the taxon pulse model

Abstract.— One-third to two-thirds of all tropical carabids, or ground beetles, are arboreal, and evolution of arboreality has been proposed to be a dead end in this group. Many arboreal carabids have unusual morphological features that have been proposed to be adaptations for life on vegetation, including large, hemispheric eyes; an elongated prothorax; long elytra; long legs; bilobed fourth tarsomeres; adhesive setae on tarsi; and pectinate claws. However, correlations between these features and arboreality have not been rigorously tested previously. I examined the evolution of arboreality and morphological features often associated with this habitat in a phylogenetic context. The number and rates of origins and losses of arboreality in carabids in the subfamily Harpalinae were inferred with parsimony and maximum-likelihood on a variety of phylogenetic hypotheses. Correlated evolution in arboreality and morphological characters was tested with concentrated changes tests, maximum-likelihood, and independent contrasts on optimal phylogenies. There is strong evidence that both arboreality and the morphological features examined originated multiple times and can be reversed, and in no case could the hypothesis of equal rates of gains and losses be rejected. Several features are associated with arboreality: adhesive setae on the tarsi, bilobed tarsomeres, and possibly pectinate claws and an elongated prothorax. Bulgy eyes, long legs, and long elytra were not correlated with arboreality and are probably not arboreal adaptations. The evolution of arboreal carabids has not been unidirectional. These beetles have experienced multiple gains and losses of arboreality and the morphological characters commonly associated with the arboreal habitat. The evolutionary process of unidirectional character change may not be as widespread as previously thought and reversal from specialized lifestyles or habitats may be common.     

Time‐limited environments affect the evolution of egg–body size allometry

Initial offspring size is a fundamental component of absolute growth rate, where large offspring will reach a given adult body size faster than smaller offspring. Yet, our knowledge regarding the coevolution between offspring and adult size is limited. In time‐constrained environments, organisms need to reproduce at a high rate and reach a reproductive size quickly. To rapidly attain a large adult body size, we hypothesize that, in seasonal habitats, large species are bound to having a large initial size, and consequently, the evolution of egg size will be tightly matched to that of body size, compared to less time‐limited systems. We tested this hypothesis in killifishes, and found a significantly steeper allometric relationship between egg and body sizes in annual, compared to nonannual species. We also found higher rates of evolution of egg and body size in annual compared to nonannual species. Our results suggest that time‐constrained environments impose strong selection on rapidly reaching a species‐specific body size, and reproduce at a high rate, which in turn imposes constraints on the evolution of egg sizes. In combination, these distinct selection pressures result in different relationships between egg and body size among species in time‐constrained versus permanent habitats.