Sex‐specific evolution of bite performance in Liolaemus lizards (Iguania: Liolaemidae): the battle of the sexes

Although differential selective pressures on males and females of the same species may result in sex‐specific evolutionary trajectories, comparative studies of adaptive radiations have largely neglected within‐species variation. In this study, we explore the potential effects of natural selection, sexual selection, or a combination of both, on bite performance in males and females of 19 species of Liolaemus lizards. More specifically, we study the evolution of bite performance, and compare evolutionary relationships between the variation in head morphology, bite performance, ecological variation and sexual dimorphism between males and females. Our results suggest that in male Liolaemus, the variation in bite force is at least partly explained by the variation in the degree of sexual dimorphism in head width (i.e. our estimate of the intensity of sexual selection), and neither bite force nor the morphological variables were correlated with diet (i.e. our proxy for natural selection). On the contrary, in females, the variation in bite force and head size can, to a certain extent, be explained by variation in diet. These results suggest that whereas in males, sexual selection seems to be operating on bite performance, in the case of females, natural selection seems to be the most likely and most important selective pressure driving the variation in head size. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 461–475.     

An analysis of the relative roles of plasticity and natural selection in the morphology and performance of a lizard (<Emphasis Type="Italic">Urosaurus ornatus</Emphasis>)

Evolutionary ecologists have devoted substantial attention to understanding which factors dictate processes of mortality within populations. Our goal was to understand the dynamics of natural selection on two performance traits (bite force and sprint speed) and associated morphological variables. We first quantified performance and morphology for a sample of marked tree lizards (Urosaurus ornatus) at the middle of the breeding season. We then sampled the same population in the nonbreeding season to determine which of the original lizards survived, and we also remeasured morphological and performance variables for surviving lizards. We found evidence for directional selection favoring fast sprinters in male lizards, but also a nonsignificant stabilizing trend that disfavored the very fastest lizards. However, we also detected substantial seasonal plasticity in bite force and head width, suggesting that an analysis of selection on only preselection (breeding season) values may be overly simplistic. Urosaurus males and females with low bite forces (and narrow heads) in the breeding season generally increased their bite forces and head widths during the nonbreeding season. In contrast, lizards that were initially strong biters in the breeding season diminished in head width and declined dramatically in bite force (up to about 35%). We suggest that seasonal plasticity could act as a retarding force for selection on performance, and could dampen seasonal and year-to-year fluctuations in selective pressures. We argue that this phenomenon may be particularly likely for performance traits important for social interactions related to breeding, such as bite force.     

Beak morphology and song features covary in a population of Darwin's finches (Geospiza fortis)

Animal mating signals evolve in part through indirect natural selection on anatomical traits that influence signal expression. In songbirds, for example, natural selection on beak form and function can influence the evolution of song features, because of the role of the beak in song production. In this study we characterize the relationship between beak morphology and song features within a bimodal population of Geospiza fortis on Santa Cruz Island, Galápagos. This is the only extant population of Darwin's finches that is known to possess a bimodal distribution in beak size. We test the hypothesis that birds with larger beaks are constrained to produce songs with lower frequencies and decreased vocal performance. We find that birds with longer, deeper, and wider beaks produce songs with significantly lower minimum frequencies, maximum frequencies and frequency bandwidths. Results from the analysis of the relationship between beak morphology and trill rate are mixed. Measures of beak morphology correlated positively with 'vocal deviation', a composite index of vocal performance. Overall these results support a resonance model of vocal tract function, and suggest that beak morphology, a primary target of ecological selection in Darwin's finches, affects the evolution of mating signals. We suggest that differences in song between the two modes of the distribution may influence mate recognition and perhaps facilitate assortative mating by beak size and population divergence.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 88 , 489–498.     

Naris and beak malformation caused by the parasitic fly, Philornis downsi (Diptera: Muscidae), in Darwin's small ground finch, Geospiza fuliginosa (Passeriformes: Emberizidae)

Parasites induce phenotypic modifications in their hosts, which can compromise host fitness. For example, the parasitic fly Philornis downsi , which was recently introduced to the Galápagos Islands, causes severe naris and beak malformation in Darwin's finches. The fly larvae feed on tissues from the nares of developing finch nestlings, thereby altering the size and shape of the nares and beak. Although the parasitism is age-specific (adult finches are not parasitized), naris and beak malformations persist into adulthood as parasite-induced malformations. We systematically examined adult populations of Darwin's small ground finch, Geospiza fuliginosa , on the islands of Santa Cruz for P. downsi -induced malformation. We found that malformed birds had significantly longer nares, and shorter, shallower beaks, than birds considered to be normal (i.e. with no nares or beak malformation). In addition, normal birds showed an isometry between naris length and beak dimensions (beak length feather and beak depth), which was not found in malformed birds. These differences suggest that beak morphology was influenced by P. downsi parasitism. Interestingly, we did not find any evidence of developmental impairment (smaller body size) or reduced foraging efficiency (lower body condition) between normal and malformed birds. Our findings of P. downsi -induced malformation raise new questions about the evolutionary trajectory and conservation status for this group of birds.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 577–585.     

QTL linkage mapping of zebra finch beak color shows an oligogenic control of a sexually selected trait

Mate choice based on sexual ornaments can impose strong selection, which raises the question of how genetic variation in ornaments is maintained. One mechanism that has been proposed is genic capture. If ornament expression is influenced by general condition and condition is under polygenic control, selection will be inefficient in removing genetic variation. Here we analyze whether the genetic architecture of beak color in a population of zebra finches supports this hypothesis. Zebra finch beak color is commonly assumed to be under strong selection by mate choice, although some of the evidence is ambiguous. We show that beak redness has a heritability of 34% in our population and that it is strongly genetically correlated between the sexes, suggesting that it is largely controlled by the same genes in males and females. We mapped variation in beak redness based on 1404 single-nucleotide polymorphism (SNP) markers genotyped in a large pedigree. We find evidence for linkage on four chromosomes (Tgu1, Tgu5, Tgu13, Tgu21), which together explain a large part of the additive genetic variance. Our finding of genomic regions with major additive effects is not consistent with directional selection and genic capture, but rather suggests a role of antagonistic pleiotropy in maintaining genetic variation.     

QTL and quantitative genetic analysis of beak morphology reveals patterns of standing genetic variation in an Estrildid finch

The intra- and interspecific diversity of avian beak morphologies is one of the most compelling examples for the power of natural selection acting on a morphological trait. The development and diversification of the beak have also become a textbook example for evolutionary developmental biology, and variation in expression levels of several genes is known to causally affect beak shape. However, until now, no genomic polymorphisms have been identified, which are related to beak morphology in birds. QTL mapping does reveal the location of causal polymorphisms, albeit with poor spatial resolution. Here, we estimate heritability and genetic correlations for beak length, depth and width and perform a QTL linkage analysis for these traits based on 1404 informative single-nucleotide polymorphisms genotyped in a four-generation pedigree of 992 captive zebra finches (Taeniopygia guttata). Beak size, relative to body size, was sexually dimorphic (larger in males). Heritability estimates ranged from 0.47 for beak length to 0.74 for beak width. QTL mapping revealed four to five regions of significant or suggestive genome-wide linkage for each of the three beak dimensions (nine different regions in total). Eight out of 11 genes known to influence beak morphology are located in these nine peak regions. Five QTL do not cover known candidates demonstrating that yet unknown genes or regulatory elements may influence beak morphology in the zebra finch.     

草原蜥两性的咬合力及头部形态特征比较

咬合力作为衡量动物生存能力的重要指标,可以在一定程度上反映动物捕食、反捕食和争夺配偶的能力。对于蜥蜴类动物而言,头部形态和咬合力大小之间常呈现显著线性关系。通过测量2018年7月采集于新疆霍城县图开沙漠的24号草原蜥(Trapelussanguinolenta)(雌13,雄11)的头部形态指标,并使用薄膜压力测试仪测定咬合力,采用单因素方差分析(ANOVA)、主成分分析、模型拟合及逐步回归4种方法探究草原蜥咬合力的两性差异及其与头部形态指标的关系。结果表明,草原蜥头体长、头长、头宽、头高、口宽和下颌长在两性个体间均无显著差异,草原蜥两性个体之间咬合力也没有显著差异。主成分分析及赤池信息模型拟合结果均显示,头长、头宽和下颌长是影响草原蜥咬合力的重要因素,逐步回归分析揭示草原蜥的咬合力主要受头宽影响。上述研究结果表明,草原蜥的咬合力受头部形态大小的影响,但两性个体之间咬合力却不存在显著差异,这与头部形态特征未表现出两性差异一致,这可能是草原蜥对灌丛生活的适应,具体而言,是头部大小与运动权衡的结果。     

Relationships between head morphology, bite performance and ecology in two species of Podarcis wall lizards

Understanding the relationship between form and function is central to our comprehension of how phenotypic diversity evolves. Traits involved in multiple activities, such as social interactions and ecological resource use, are under the influence of different evolutionary forces potentially acting in opposite directions. Such systems provide the opportunity of understanding how potential constraints on morphological variation may influence whole-organism performance. In this study we examined morphology and bite performance in two closely related species of Podarcis wall lizards with divergent microhabitat preferences, to investigate how natural and sexual selection interact to shape the evolution of head traits. Our results show that although head morphology is markedly different between species and sexes, only sexes differ in bite force, indicating that the ecological differentiation between species is reflected in their morphology but does not constrain performance. Rather, the modification of the relative size of head components between species and a shift in the form-function relationship provide a potential explanation of how equal performance is attained by different morphological configurations. Geometric morphometrics provide a clear, biomechanically meaningful image of how this is achieved and show a bisexual pattern of head shape-bite force association in both species. This, together with a strong allometry of head size on body size and head shape on head size, provides indirect morphological evidence for the importance of sexual selection in shaping morphological and functional patterns. Finally, our findings suggest that the differences observed between species and sexes in head traits and bite performance are not reflected in their dietary ecology, implying that if trophic niche segregation between groups occurs, the reasons behind it are not primarily related to head morphology and functional variation.     

The adaptive genomic landscape of beak morphology in Darwin's finches

Beak shape in Darwin's ground finches (Geospiza) is emblematic of natural selection and adaptive radiation, yet our understanding of the genetic basis of beak shape variation, and thus the genetic target of natural selection, is still evolving. Here we reveal the genomic architecture of beak shape variation using genomewide comparisons of four closely related and hybridizing species across 13 islands subject to parallel natural selection. Pairwise contrasts among species were used to identify a large number of genomic loci that are consistently related to species differences across a complex landscape. These loci are associated with hundreds of genes that have enriched GO categories significantly associated with development. One genomic region of particular interest is a section of Chromosome 1A with many candidate genes and increased linkage. The distinct, pointed beak shape of the cactus finch is linked to an excess of intermediate frequency alleles and increased heterozygosity in significant SNPs, but not across the rest of the genome. Alleles associated with pointier beaks among species were associated with pointier‐beaked populations within each species, thus establishing a common basis for natural selection, species divergence and adaptive radiation. The adaptive genomic landscape for Darwin's finches mirrors theoretical expectations based on morphological variation. The implication that a large number of genes are actively maintained to facilitate beak variation across parallel populations with documented interspecies admixture challenges our understanding of evolutionary processes in the wild.     

Sex,androgens, and whole‐organism performance in an Australian lizard

Understanding underlying physiological differences between the sexes in circulating androgens and how hormonal variation affects morphology–performance relationships may help clarify the evolution of sexual dimorphism in diverse taxa. Using a widely distributed Australian lizard (Eulamprus quoyii) with weak sexual dimorphism and no dichromatism, we tested whether circulating androgens differed between the sexes and whether they covaried with morphological and performance traits (bite force, sprint speed, endurance). Males had larger head dimensions, stronger bite force, faster sprint speed, and longer endurance compared to females. We found that the sexes did not differ in androgen concentrations and that androgens were weakly associated with both morphological and performance traits. Interestingly, high circulating androgens showed a nonlinear relationship with bite force in males and not females, with this relationship possibly being related to alternative male reproductive tactics. Our results suggest that androgens are not strongly correlated with most performance and morphological traits, although they may play an important organizational role during the development of morphological traits, which could explain the differences in morphology and thus performance between the sexes. Differences in performance between the sexes suggest differential selection on these functional traits between males and females. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111, 834–849.     

Morphological variation in the Cape Dwarf Chameleon (Bradypodion pumilum) as a consequence of spatially explicit habitat structure differences

An organism's phenotype is to some extent influenced by costs and benefits in terms of natural and sexual selection. The intensity of natural selection can in part be driven by habitat structure, which may result in varying levels of crypsis and/or selection on traits related to maximizing performance in that habitat. This may be countered by sexual selection, which can lead to sexual dimorphism in body size and/or the expression of conspicuous ornamentation relating to maximizing reproductive success. The intensity of these forces can also be different between the sexes, resulting in complex patterns of phenotypic variation. With this in mind, we examined morphological variation within the Cape Dwarf Chameleon, Bradypodion pumilum. The species inhabits two geographically disjunct habitat types and, in the present study, we demonstrate that chameleons from the two habitats show morphological differences. Large, conspicuous individuals inhabit closed vegetation, whereas small, drab individuals inhabit open vegetation. However, when morphological traits are size‐adjusted, the open vegetation morph displays many traits that are larger for its body size than the closed vegetation morph, especially for characters related to locomotion (limbs) and bite force (head width). Sexual dimorphism is also present, although the degree and number of dimorphic characters was very different between the two morphs, with size‐adjusted male‐biased dimorphism much more pronounced in the closed morph. Overall, our findings suggest that natural selection in open habitats limits both body size and conspicuous characters, although sexual selection in closed habitats favours the development of ornamentation related to display. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 878–888.     

Exploring possible human influences on the evolution of Darwin's finches

Humans are an increasingly common influence on the evolution of natural populations. Potential arenas of influence include altered evolutionary trajectories within populations and modifications of the process of divergence among populations. We consider this second arena in the medium ground finch (Geospiza fortis) on Santa Cruz Island, Galápagos, Ecuador. Our study compared the G. fortis population at a relatively undisturbed site, El Garrapatero, to the population at a severely disturbed site, Academy Bay, which is immediately adjacent to the town of Puerto Ayora. The El Garrapatero population currently shows beak size bimodality that is tied to assortative mating and disruptive selection, whereas the Academy Bay population was historically bimodal but has lost this property in conjunction with a dramatic increase in local human population density. We here evaluate potential ecological-adaptive drivers of the differences in modality by quantifying relationships between morphology (beak and head dimensions), functional performance (bite force), and environmental characteristics (diet). Our main finding is that associations among these variables are generally weaker at Academy Bay than at El Garrapatero, possibly because novel foods are used at the former site irrespective of individual morphology and performance. These results are consistent with the hypothesis that the rugged adaptive landscapes promoting and maintaining diversification in nature can be smoothed by human activities, thus hindering ongoing adaptive radiation.     

Morphology,ornaments and performance in two chameleon ecomorphs: is the casque bigger than the bite?

The evolution of ecomorphs within a species may represent either unique evolutionary events or multiple convergent events in similar environments. Functional studies of differing morphological traits of ecomorphs have been important to elucidate their role in adaptive radiations. The Cape dwarf chameleon, Bradypodion pumilum, has two ecomorphs: a large, brightly colored, ornate form found in closed habitats, and a small, dull form with reduced ornamentation found in open vegetation. The typical form is known to use casque size to communicate fighting ability, but it is unknown whether this is an honest signal and whether casque size is related to bite force. We show through a population genetic analysis that these ecomorphs are not separate genetic lineages but the result of multiple transitions between closed and open habitats. From measurements of ornamental and non-ornamental morphological characters and bite force in 105 chameleons, we find that bite force is significantly related to head size and is best predicted by head width. Bite force was reasonably predicted by casque height in ecomorphs from closed habitats, but not in those from open habitats. For size-adjusted data, open habitat males had wider heads, biting harder than closed habitat males. Our data suggest honesty in signaling for closed habitat ecomorphs, but for open habitat ecomorphs communication is different, a finding commensurate with the common framework for species radiations.     

Non-random fitness variation in two populations of Darwin's finches

Darwinian fitness of an individual is measured by the number of recruits it contributes to the next generation. We studied variation in fitness among members of three cohorts of two species of Darwin's finches living on the Galipagos island of Daphne Major: the medium ground finch (Geospiza fortis) and cactus finch (Geospiza scandens). Individuals of both species live for up to 16 years. Variation in fitness was neither random nor heritable. Non-randomness arises as a result of a few individuals living for an exceptionally long time and breeding many times. For each cohort, the number of recruits per breeder is strongly predicted by the number of fledglings per breeder. In turn, the number of fledglings is strongly predicted by longevity of the breeder. These results suggest that the most important determinant of fitness is the ability of an individual to survive to breed in many years. Morphological traits affect this ability. Although morphological traits are heritable they do not change unidirectionally because they are selected in opposite directions, and in different combinations, under fluctuating environmental conditions. Non-random fitness variation in fluctuating populations implies much smaller genetically effective sizes than breeding population sizes.     

The fitness advantage of a high-performance weapon

Weapons used in combat between males are usually attributed to sexual selection, which operates via a fitness advantage for males with weapons of better 'quality'. Because the performance capacity of morphological traits is typically considered the direct target of selection, Darwin's intrasexual selection hypothesis can be modified to predict that variation in reproductive success should be explained by variation in performance traits relevant to combat. Despite such a straightforward prediction, tests of this hypothesis are conspicuously lacking. We show that territorial male collared lizards with greater bite-force capacity sire more offspring than weaker biting rivals but exhibit no survival advantage. We did not detect stabilizing or disruptive selection on bite-force capacity. Taken together, these results support the hypothesis that superior weapon performance provides a fitness advantage through increased success in male contests. Sexual selection on weapon performance therefore appears to be a force driving the evolution and maintenance of sexual dimorphism in head shape.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 840–845.     

Sexual dimorphism,body size,bite force and male mating success in tuatara

Sexual dimorphisms in body size and head size are common among lizards and are often related to sexual selection on male fighting capacity (organismal performance) and territory defence. However, whether this is generally true or restricted to lizards remains untested. Here we provide data on body and head size, bite performance and indicators of mating success in the tuatara (Sphenodon punctatus), the closest living relative to squamates, to explore the generality of these patterns. First, we test whether male and female tuatara are dimorphic in head dimensions and bite force, independent of body size. Next, we explore which traits best predict bite force capacity in males and females. Finally, we test whether male bite force is correlated with male mating success in a free‐ranging population of tuatara (Sphenodon punctatus). Our data confirm that tuatara are indeed dimorphic in head shape, with males having bigger heads and higher bite forces than females. Across all individuals, head length and the jaw closing in‐lever are the best predictors of bite force. In addition, our data show that males that are mated have higher absolute but not relative bite forces. Bite force was also significantly correlated to condition in males but not females. Whereas these data suggest that bite force may be under sexual selection in tuatara, they also indicate that body size may be the key trait under selection in contrast to what is observed in squamates that defend territories or resources by biting. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 287–292.     

The allopatric phase of speciation: the sharp-beaked ground finch (Geospiza difficilis) on the Galápagos islands

Using microsatellite DNA variation, morphological measurements and sonagrams made from tape-recordings in the field, we examine die allopatric differentiation of six populations of the sharp-beaked ground finch, Geospiza difficilis , in the Galapagos archipelago. We ask how and why die populations became differentiated, and consider what die differences imply about speciation. An important factor is time; G. difficilis is one of the phylogenetically oldest species. Populations became differentiated by adapting in beak morphology to different food supplies. Since beak size and shape also function in conspecific mate recognition and choice, die potential for reproductive isolation from sister and parental taxa arose as a correlated effect of natural selection on resource-exploiting traits. This conforms to a standard explanation for the origin of pre-mating isolation as a byproduct of adaptive changes in allopatry without being adaptive itself. However, diis explanation is incomplete. Vocal characteristics also differentiated, partly as a result of natural and sexual selection independent of beak size change in environments with different sound transmitting properties. An additional element of chance is indicated by a comparison of closely-related populations on two islands, Wolf and Darwin, that are geographically close, and topographically and floristically similar. The populations have markedly different vocalizations. Morphological characters, vocalizations and genetic traits do not vary concordandy among die six populations. One population (Genovesa) is genetically more similar to other congeneric species. Phenotypic similarities with G. difficilis are the result of a uniquely long retention of shared ancestral traits. Arguments under the phylogenetic species concept justify recognizing this population as a separate species, Geospiza acutirostris. Under the biological species concept it should remain as currentiy classified, G. difficilis.     

Fission and fusion of Darwin's finches populations

This study addresses the causes and evolutionary consequences of introgressive hybridization in the sympatric species of Darwin's ground finches (Geospiza) on the small island of Daphne Major in the Galápagos archipelago. Hybridization occurs rarely (less than 2% of breeding pairs) but persistently across years, usually as a result of imprinting on the song of another species. Hybrids survive well under some ecological conditions, but not others. Hybrids mate according to song type. The resulting introgression increases phenotypic and genetic variation in the backcrossed populations. Effects of introgression on beak shape are determined by the underlying developmental genetic pathways. Introgressive hybridization has been widespread throughout the archipelago in the recent past, and may have been a persistent feature throughout the early history of the radiation, episodically affecting both the speed and direction of evolution. We discuss how fission through selection and fusion through introgression in contemporary Darwin's finch populations may be a reflection of processes occurring in other young radiations. We propose that introgression has the largest effect on the evolution of interbreeding species after they have diverged in morphology, but before the point is reached when genetic incompatibilities incur a severe fitness cost.     

Evolution of bite performance in turtles

Abstract Among vertebrates, there is often a tight correlation between variation in cranial morphology and diet. Yet, the relationships between morphological characteristics and feeding performance are usually only inferred from biomechanical models. Here, we empirically test whether differences in body dimensions are correlated with bite performance and trophic ecology for a large number of turtle species. A comparative phylogenetic analysis indicates that turtles with carnivorous and durophagous diets are capable of biting harder than species with other diets. This pattern is consistent with the hypothesis that an evolutionary increase in bite performance has allowed certain turtles to consume harder or larger prey. Changes in carapace length tend to be associated with proportional changes in linear head dimensions (no shape change). However, maximum bite force tends to change in proportion to length cubed, rather than length squared, implying that changes in body size are associated with changes in the design of the jaw apparatus. After the effect of body size is accounted for in the analysis, only changes in head height are significantly correlated with changes in bite force. Additionally, our data suggest that the ability to bite hard might trade off with the ability to feed on fast agile prey. Rather than being the direct result of conflicting biomechanical or physiological demands for force and speed, this trade‐off may be mediated through the constraints imposed by the need to retract the head into the shell for defensive purposes.     

Sexual Dimorphism in Bite Performance Drives Morphological Variation in Chameleons

Phenotypic performance in different environments is central to understanding the evolutionary and ecological processes that drive adaptive divergence and, ultimately, speciation. Because habitat structure can affect an animal’s foraging behaviour, anti-predator defences, and communication behaviour, it can influence both natural and sexual selection pressures. These selective pressures, in turn, act upon morphological traits to maximize an animal’s performance. For performance traits involved in both social and ecological activities, such as bite force, natural and sexual selection often interact in complex ways, providing an opportunity to understand the adaptive significance of morphological variation with respect to habitat. Dwarf chameleons within the Bradypodion melanocephalum-Bradypodion thamnobates species complex have multiple phenotypic forms, each with a specific head morphology that could reflect its use of either open- or closed-canopy habitats. To determine whether these morphological differences represent adaptations to their habitats, we tested for differences in both absolute and relative bite performance. Only absolute differences were found between forms, with the closed-canopy forms biting harder than their open-canopy counterparts. In contrast, sexual dimorphism was found for both absolute and relative bite force, but the relative differences were limited to the closed-canopy forms. These results indicate that both natural and sexual selection are acting within both habitat types, but to varying degrees. Sexual selection seems to be the predominant force within the closed-canopy habitats, which are more protected from aerial predators, enabling chameleons to invest more in ornamentation for communication. In contrast, natural selection is likely to be the predominant force in the open-canopy habitats, inhibiting the development of conspicuous secondary sexual characteristics and, ultimately, enforcing their overall diminutive body size and constraining performance.