Head shape allometry and proximate causes of head sexual dimorphism in Podarcis lizards: joining linear and geometric morphometrics

Podarcis bocagei and Podarcis carbonelli are two lacertid species endemic to the western Iberian Peninsula, and both show head size and shape sexual dimorphism. We studied immature and adult head sexual dimorphism and analysed ontogenetic trajectories of head traits with body and head size, aiming to shed light on the proximate mechanisms involved. Immatures were much less dimorphic than adults, but geometric morphometric techniques revealed that head shape sexual differences are already present at this stage. Males and females differed in allometry of all head characters with body size, with males showing a disproportionate increase of head size and dimensions. On the other hand, head dimensions and head shape changed with increasing head size following similar trends in both sexes, possibly indicating developmental restrictions. Consequently, adult sexual dimorphism for head characters in these species is the result of both shape differences in the immature stage and hypermetric growth of the head in relation to body size in males.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 111–124.     

Size dimorphism in Rankinia [Tympanocryptis] diemensis (Family Agamidae): sex-specific patterns and geographic variation

Sexual dimorphism has implications for a range of biological and ecological factors, and intersexual morphological differences within a species provide an ideal opportunity for investigating evolutionary influences on phenotypic variation. We investigated sexual size dimorphism (SSD) in an agamid species, Rankinia [Tympanocryptis] diemensis , to determine whether overall size and/or relative morphological trait size differences exist and whether geographic variation in size dimorphism occurs in this species. Relative morphological trait proportions included a range of head, limb, and inter-limb measurements. We found significant overall intersexual adult size differences; females were the larger sex across all sites but the degree of dimorphism between the sexes did not differ between sites. This female-biased size difference is atypical for agamid lizards, which are usually characterized by large male body size. In this species, large female-biased SSD appears to have evolved as a result of fecundity advantages. The size of relative morphological trait also differed significantly between the sexes, but in the opposite direction: relative head, tail, and limb sizes were significantly larger in males than females. This corresponds to patterns in trait size usually found in this taxonomic group, where male head and limb size is important in contest success such as male–male rivalry. There were site-specific morphological differences in hatchlings, including overall body size, tail, inter-limb, thigh, and hindlimb lengths; however, there were no sex-specific differences indicating the body size differences present in the adult form occur during ontogeny.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 699–709.     

Functional basis for sexual differences in bite force in the lizard Anolis carolinensis

In many species of lizards, males attain greater body size and have larger heads than female lizards of the same size. Often, the dimorphism in head size is paralleled by a dimorphism in bite force. However, the underlying functional morphological basis for the dimorphism in bite force remains unclear. Here, we test whether males are larger, and have larger heads and bite forces than females for a given body size in a large sample of Anolis carolinensis . Next, we test if overall head shape differs between the sexes, or if instead specific aspects of skull shape can explain differences in bite force. Our results show that A. carolinensis is indeed dimorphic in body and head size and that males bite harder than females. Geometric morphometric analyses show distinct differences in skull shape between males and females, principally reflecting an enlargement of the jaw adductor muscle chamber. Jaw adductor muscle mass data confirm this result and show that males have larger jaw adductors (but not jaw openers) for a given body and head size. Thus, the observed dimorphism in bite force in A. carolinensis is not merely the result of an increase in head size, but involves distinct morphological changes in skull structure and the associated jaw adductor musculature.  © 2007 The Linnean Society of London, Biological Journal of the Linnean Society , 2007, 91 , 111–119.     

Sex-specific niche partitioning and sexual size dimorphism in Australian pythons (Morelia spilota imbricata)

Sexual dimorphism is usually interpreted in terms of reproductive adaptations, but the degree of sex divergence also may be affected by sex-based niche partitioning. In gape-limited animals like snakes, the degree of sexual dimorphism in body size (SSD) or relative head size can determine the size spectrum of ingestible prey for each sex. Our studies of one mainland and four insular Western Australian populations of carpet pythons ( Morelia spilota ) reveal remarkable geographical variation in SSD, associated with differences in prey resources available to the snakes. In all five populations, females grew larger than males and had larger heads relative to body length. However, the populations differed in mean body sizes and relative head sizes, as well as in the degree of sexual dimorphism in these traits. Adult males and females also diverged strongly in dietary composition: males consumed small prey (lizards, mice and small birds), while females took larger mammals such as possums and wallabies. Geographic differences in the availability of large mammalian prey were linked to differences in mean adult body sizes of females (the larger sex) and thus contributed to sex-based resource partitioning. For example, in one population adult male snakes ate mice and adult females ate wallabies; in another, birds and lizards were important prey types for both sexes. Thus, the high degree of geographical variation among python populations in sexually dimorphic aspects of body size and shape plausibly results from geographical variation in prey availability.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77 , 113–125.     

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 in lizard body shape: the roles of sexual selection and fecundity selection

Sexual dimorphism is widespread in lizards, with the most consistently dimorphic traits being head size (males have larger heads) and trunk length (the distance between the front and hind legs is greater in females). These dimorphisms have generally been interpreted as follows: (1) large heads in males evolve through male-male rivalry (sexual selection); and (2) larger interlimb lengths in females provide space for more eggs (fecundity selection). In an Australian lizard (the snow skink, Niveoscincus microlepidotus), we found no evidence for ongoing selection on head size. Trunk length, however, was under positive fecundity selection in females and under negative sexual selection in males. Thus, fecundity selection and sexual selection work in concert to drive the evolution of sexual dimorphism in trunk length in snow skinks.     

Sexual dimorphism of heads and abdomens: Different approaches to ‘being large’ in female and male lizards

Sexual‐size dimorphism (SSD) is widespread in animals. Body length is the most common trait used in the study of SSD in reptiles. However, body length combines lengths of different body parts, notably heads and abdomens. Focusing on body length ignores possible differential selection pressures on such body parts. We collected the head and abdomen lengths of 610 lizard species (Reptilia: Squamata: Sauria). Across species, males have relatively larger heads, whereas females have relatively larger abdomens. This consistent difference points to body length being an imperfect measure of lizard SSD because it comprises both abdomen and head lengths, which often differ between the sexes. We infer that female lizards of many species are under fecundity selection to increase abdomen size, consequently enhancing their reproductive output (enlarging either clutch or offspring size). In support of this, abdomens of lizards laying large clutches are longer than those of lizards with small clutches. In some analyses, viviparous lizards have longer abdomens than oviparous lizards with similar head lengths. Our data also suggest that male lizards are under sexual selection to increase head size, which is positively related to winning male–male combats and to faster grasping of females. Thus, larger heads could translate into higher probability to mate. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 110 , 665–673.     

Functional and ecological relevance of intraspecific variation in body size and shape in the lizard Podarcis melisellensis (Lacertidae)

Within populations, individual animals may vary considerably in morphology and ecology. The degree to which variation in morphology is related to ecological variation within a population remains largely unexplored. We investigated whether variation in body size and shape among sexes and age classes of the lizard Podarcis melisellensis translates in differential whole-animal performance (sprint speed, bite force), escape and prey attack behaviour in the field, microhabitat use and diet. Male and female adult lizards differed significantly in body size and head and limb proportions. These morphological differences were reflected in differences in bite strength, but not in sprint speed. Accordingly, field measurements of escape behaviour and prey attack speed did not differ between the sexes, but males ate larger, harder and faster prey than females. In addition to differences in body size, juveniles diverged from adults in relative limb and head dimensions. These shape differences may explain the relatively high sprint and bite capacities of juvenile lizards. Ontogenetic variation in morphology and performance is strongly reflected in the behaviour and ecology in the field, with juveniles differing from adults in aspects of their microhabitat use, escape behaviour and diet.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 251–264.     

Sexual dimorphism and interpopulation differences in lizard hind limb length: locomotor performance or chemical signalling?

Intraspecific variation in morphology has often been related to fitness differences through its effects on performance. In lizards, variation in hind limb length can be shaped by natural selection for increased locomotor performance, sexual selection on the number or size of femoral pores involved in chemical signalling, or both. Here, we analyse the selective forces involved in sexual dimorphism and differences in hind limb length between two populations of Psammodromus algirus living at different elevation. Males were more robust and had longer hind limbs and limb segments than females, and low‐elevation lizards had longer limbs than high‐elevation lizards. However, differences in locomotor performance were small and non‐significant, making natural selection for faster runs an unlikely explanation for the observed pattern. On the other hand, males had more femoral pores than females, and lizards had more pores at lower elevation, although the difference was significant only for males (which invest more in chemical signalling). In males, the number of pores, which remains constant along a lizard's life, was not correlated with hind limb length. However, femur length was positively correlated with mean pore size, allowing low‐elevation males to have larger than expected pores, which could increase the effectiveness with which they spread their signals in a dry and warm habitat where chemicals become volatile rapidly. Also, saturation of the sexual coloration of the head was higher for low‐elevation males, suggesting that sexual selection pressures may be more intense. Overall, our results indicate that sexual selection plays a significant role in shaping intraspecific variation in hind limb length. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 318–329.     

Factors shaping the evolution of colour patterns in Australian agamid lizards (Agamidae): a comparative study

Identifying general patterns of adaptive coloration in animals can help to elucidate the evolutionary processes that generate them. We examined the evolution of colour patterns in Australian agamid lizards, a morphologically and ecologically diverse group that relies primarily on visual communication. We tested whether certain types of colour (yellow–reds and black) were likely to be used as sexual signals, as indicated by their association with indices of sexual selection, namely, sexual dichromatism and sexual dimorphism in body size and head shape. We then tested whether sexually dichromatic colours are associated with specific patterns (uniform, mottled, striped, blotched, reticulated) or ecological variables such as habitat openness, arboreality, and substrate type. The presence of yellow–red on lateral and ventral body regions and black on ventral body regions was significantly more common in males than females. Lateral yellow–red in males was associated with the total extent of sexual dichromatism and size dimorphism, whereas ventral yellow–red was associated with sexual dichromatism. Both lateral and ventral yellow–red were associated with uniform patterning, suggesting that sexual signals in male agamid lizards may often comprise uniform patches or flushes of yellow–red. Although ventral black coloration was more prevalent on males (i.e. strongly sexually dichromatic), it was not associated with indices of sexual selection, suggesting that, in agamid lizards, yellow–red coloration is more likely to be sexually selected than black. Sexually dichromatic coloration was not strongly associated with any of the ecological variables measured. We found some associations, however, between female dorsal patterns and ecological variables, suggesting that female patterns are influenced by natural selection. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 101–112.     

Size-dependent mating strategies and the risk of cannibalism

The role of sexual selection in determining the nature and direction of sexual size dimorphism may depend upon the timing of sexual selection, and this may also influence the variation in male size. For example, selection through sperm competition favours smaller males in the highly sexually size dimorphic orb-weaving spider Nephila edulis , whereas larger males are better able to exclude their smaller rivals from the central hub of the web where mating takes place. We investigate experimentally the role of body size and hub tenure in determining male fertilization success when males of different sizes compete for a single female over a 24-h period that includes a period of darkness. Our results confirm that small and large males obtain similar paternity share but that, in contrast with previous studies, hub tenure does not translate into greater paternity share. Unexpectedly, smaller males are at greater risk of postmating sexual cannibalism than larger males, suggesting that natural selection through sexual cannibalism may place a lower limit on male size.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 94 , 355–363.     

Diversity and evolution of male secondary sexual characters in African squeakers and long-fingered frogs

The African frog genera Arthroleptis and Cardioglossa are unique among vertebrates in having males with extremely long third fingers. In some species, this sexual dimorphism is impressive, with male third fingers approaching 40% of body length. However, the diversity of this trait has not been documented thoroughly and several species appear to lack this trait. The present study documents the diversity of male secondary sexual traits in Arthroleptis and Cardioglossa , including elongate third fingers and digital and inguinal spines. Furthermore, it explores hypotheses of trait evolution, including explanations for the absence of male traits. Analyses of covariance suggest that the functional relationship between finger length and snout–vent length (SVL), both within and among species, is different for male finger III than for male fingers I, II, and IV, or for female finger III. Ancestral state reconstruction suggests that all male traits were present in the most recent common ancestor of Arthroleptis and Cardioglossa and that reduction or loss of traits occurred later. Across species, independent contrast analyses find no correlation between SVL and either male relative third digit length or dimorphism in relative third digit length. The number of spines on male fingers II and III are positively correlated but spine number is not correlated with SVL and only weakly correlated with relative third digit length. The diversity of male traits is evolutionarily labile and is not explained by simple hypotheses of character evolution. Arthroleptis and Cardioglossa may thus provide an interesting study system for understanding how changes in sexual selection forces produce male trait diversity.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 553–573.     

Context‐dependent expression of sexual dimorphism in island populations of the common wall lizard (Podarcis muralis)

The condition‐dependent sexual dimorphism model explains the evolution and maintenance of sexual dimorphism in traits targeted by sexual selection, and predicts that the magnitude of sexual dimorphism depends on the variability of individual condition, male traits being more variable than female corresponding traits. Most convincing examples concern insects, while studies among vertebrates are scanty because manipulating condition often is not possible, and the time to reach sexual maturity may be too long. Islands offer a unique opportunity to compare how the environment affects the expression of sexual dimorphism, since they represent ‘natural experimental sets’ in which different populations of the same species may experience alternative environmental constraints. We investigated the occurrence of context‐dependent expression in sexual dimorphism of head shape in insular populations of the common wall lizards (Podarcis muralis) inhabiting the Tuscan Archipelago (Tyrrhenian Sea). Alternative models were formulated: H₀ assumes that the sexual dimorphism is uninfluenced by islands, H₁ assumes the only effect of phylogeny, H_2A and H_2B account for the biogeography of the archipelago (island size and distance from the mainland), while H₃ assumes island‐specific effects on sexual dimorphism. Models were compared using Akaike's information criterion adjusted for multivariate analyses. All hypotheses performed better than H₀, but H₃ largely outperformed all other alternative hypotheses, indicating that environmental features of islands play an additive effect to ontogenetic, biogeographic and genetic factors in defining variation in head shape sexual dimorphism. Our results support the hypothesis of a context‐dependent sexual dimorphism in common wall lizards. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 552–565.     

Quantification of sexual dimorphism in Asellus aquaticus (Crustacea: Isopoda) using outline approaches

A marked sexual dimorphism is often observed in arthropods species in which males perform precopulatory mate guarding. It is generally thought to reflect the influence of sexual selection. Until now, sexual dimorphisms associated with mate guarding have mainly been qualitatively described. However, assessing the effects of sexual selection on sexual dimorphims requires a preliminary quantitative assessment of differences in morphology between sexes. Using Fourier analyses, we tested if morphological dimorphisms could be quantitatively assessed in the isopod Asellus aquaticus . In addition, we checked whether sexual dimorphism in shape was exclusively related to mate guarding through considering characters that are not, a priori , implicated in mating behaviour. To assess the potential role of sexual selection in shaping morphology, we then examined how dimorphic characters could influence males' pairing success. Three characters (pleotelson, paraeopods 4 and 5) differed significantly in shape between males and females. In addition, two characters (pleotelson and paraeopods 4) differed in shape between guarding males and non-guarding males, with the latter being closer in shape to females. This suggests that sexual selection may be partly responsible for the observed morphological divergence between sexes in A. aquaticus .  © 2002 The Linnean Society of London, Biological Society of the Linnean Society , 2002, 77 , 523–533.     

Female-biased sexual size dimorphism in tinamous: a comparative test fails to support Rensch's rule

Rensch's rule states that degree of sexual dimorphism increases with body size in species with larger males, and decreases with body size in those with larger females. To test this rule, we assessed the pattern of sexual size dimorphism in tinamous using a comparative analysis of independent contrasts. Tinamous are a monophyletic group of primitive birds comprising at least 47 ground dwelling species with prominent or exclusive paternal care of eggs and offspring. Although the size of females exceeded that of males in most considered species, we found an isometric relationship between males and females, instead of the negative allometric one predicted by Rensch's rule. Previous studies in Strigiformes and Falconiformes found positive allometric and isometric relationships respectively, and, considering these findings with our results, we conclude that Rensch's rule is not supported by birds with exclusively female-biased sexual dimorphism in size.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 80 , 519–527     

Differential sexual dimorphism: size and shape in the cranium and pelvis of grey foxes (Urocyon)

Patterns of sexual size dimorphism (SSD) and cranial dimorphism are well documented. However, limited examinations exist of the contrasts in the patterns and nature of dimorphism across body regions (e.g. cranium, pelvis), particularly when these regions have different sex-specific functions (e.g. display in mating, locomotion, and reproduction). Using landmark-based morphometric techniques, we investigated size and shape dimorphism variation in the crania and pelves of two closely-related fox species within the genus Urocyon . Although we found no significant size and shape dimorphism in the crania of either species, we did find significant dimorphism in the pelvis: its size was dimorphic in Urocyon littoralis (but not in Urocyon cinereoargenteus ) and its shape was dimorphic in both species (though more pronounced in U. littoralis ). The observation of greater dimorphism in the pelvis than in the cranium suggests that factors such as offspring size and locomotor mode play a greater role in sexual dimorphism than simple 'whole body' allometric affects associated with dimorphism in body size.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 96 , 339–353.     

Which proximate factor determines sexual size dimorphism in tiger snakes?

Diverse interactions between factors that influence body size complicate the identification of the primary determinants of sexual size dimorphism. Using data from a long‐term field study (1997–2009), we examined the contributions of the main proximate factors potentially influencing sexual size dimorphism from birth to adulthood in tiger snakes (Notechis scutatus). Data on body size, body mass and body condition of neonates, juveniles and adults were obtained by mark–recapture. Frequent recaptures allowed us to monitor reproductive status, diet and food intake, and to estimate survival and growth rates in age and sex classes. Additional data from females held briefly in captivity enabled us to assess reproductive output and the body mass lost at parturition (proxies for reproductive effort). From birth to maturity, individuals of both sexes experienced similar growth and mortality rates. We found no difference in diet, feeding and survival rates between the sexes, nor between juveniles and adults. On maturity, despite comparable diet and food intake by both sexes, the high energy requirements of vitellogenesis and gestation were responsible for a depletion of body reserves and probably resulted in a marked decrease in growth rates. Males were largely exempt from such costs of reproduction, and so could grow faster than females and attain larger body sizes. The absence of niche divergence between the sexes (uniformity of habitat, lack of predators) suggests that the impact of differential energetic investment for reproduction on growth rate is probably the main proximate factor influencing sexual size dimorphism in this species. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 668–680.     

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.     

Limits to sexual size dimorphism in red‐winged blackbirds: the cost of getting big?

A fundamental assumption of sexual selection theory is that the reproductive advantage of large size is balanced by a survival disadvantage. Previous studies of the sexually size-dimorphic red-winged blackbird ( Agelaius phoeniceus ) have indicated that the largest adult males have a survival advantage, suggesting that the limit to male size may be the cost of getting big rather than the cost of being big. If the cost of getting big limits male size, then starvation rates for male nestlings should exceed those of female nestlings. In addition, given high heritability of body size, larger parents should lose more nestlings, particularly males, to starvation. We tested these predictions for red-winged blackbirds using data on the sex of 1356 fledglings from 465 nests collected over 10 years. We found no disadvantage for male nestlings relative to females – 49% of fledglings were male and previous research had shown that 48% of hatchlings are male. We also found no disadvantage for male nestlings that would become large adults (i.e. those with larger parents) – partial brood loss and fledging sex ratios did not vary with mid-parent size. Given no apparent disadvantage to large size for males either as adults or as nestlings, this leaves only the period between fledging and adulthood during which natural selection might limit sexual size dimorphism, although other mechanisms might explain the failure to find a limit to male size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 353–361.     

Morphological, functional and evolutionary aspects of tail autotomy and regeneration in the 'living fossil'Sphenodon (Reptilia: Rhynchocephalia)

Tail autotomy and regeneration are less known in Sphenodon ('Reptilia': Rhynchocephalia) than in Squamata. We examined museum specimens, Sphenodon guntheri ( N  = 8) and Sphenodon punctatus ( N  = 172), wild Sphenodon punctatus ( N  = 19) and Sphenodon sp. skeletons ( N  = 8). In S. punctatus , unlike in typical Squamata, sexes had similar relative (intact) tail lengths, and regeneration frequencies; tail and body growth was isometric. Tail breakage was usually intravertebral, usually followed by ablation of a variably sized terminal vertebral piece, partly deviating from lizards. Hypothetically, imperfect autotomy results from sphenodon's primitiveness. As in squamates, tail-losers were morphologically more left-side dominant than tail-retainers. Individual directional asymmetries in digit morphology and in digit injury were correlated (in lizards observed only at population level); tail-losers had more fluctuating asymmetry but their exclusion did not facilitate morphological taxonomic distinctions (no 'Seligmann effect'). In S. punctatus , extents and directions of sexual dimorphism paralleled differences between tail-retainers and tail-losers, females resembling tail-losers, also accounting for character interdependence (developmental constraints; employing a method similar to phylogenetic contrasts). The variation in the location of tail injury was correlated with the continuum of variation between injured and intact (pholidotic) morphotypes. These last two phenomena remain to be explored in Squamates.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 721–743.