Patterns of sexual size dimorphism in Chelonia: revisiting Kinosternidae

Rensch's rule, a macroevolutionary pattern in which sexual size dimorphism (SSD) increases with body size in male‐biased SSD species, or decreases with female‐biased SSD species, has been investigated in many vertebrates because it indicates whether SSD is being driven by sexual selection or a different force (i.e. fecundity or natural selection). Evidence in turtles has shown some conflicting results, which may be explained by the different phylogenies used in the analyses. Because the newly available well‐resolved phylogeny of family Kinosternidae provides evidence for the ancient monophyly of Staurotypidae and Kinosternidae and their recognition as separate families (previously Staurotypidae was considered as a subfamily within Kinosternidae) and introduced the genus Cryptochelys for the monophyletic leucostomum clade, we revisit the pattern of SSD and body size in Kinosternidae. By contrast to what had been proposed, we found that the Kinosternidae as formerly recognized (i.e. including Staurotypus and Claudius) and the restricted Kinosternidae both follow a pattern consistent with Rensch's rule. Our analysis with published body size data did not change our results, confirming the importance of the phylogeny used in macroevolutionary studies. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 806–809.     

Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size

Phylogenetic comparative methods were used to analyze the consequences of sexual selection on canine size and canine size dimorphism in primates. Our analyses of previously published body mass and canine size data revealed that the degree of sexual selection is correlated with canine size dimorphism, as well as with canine size in both sexes, in haplorhine but not in strepsirrhine primates. Consistent with these results, male and female canine size was found to be highly correlated in all primates. Since canine dimorphism and canine size in both sexes in haplorhines were found to be not only related to mating system but also to body size and body size dimorphism (characters which are also subject to or the result of sexual selection), it was not apparent whether the degree of canine dimorphism is the result of sexual selection on canine size itself, or whether canine dimorphism is instead a consequence of selection on body size, or vice versa. To distinguish among these possibilities, we conducted matched-pairs analyses on canine size after correcting for the effects of body size. These tests revealed significant effects of sexual selection on relative canine size, indicating that canine size is more important in haplorhine male-male competition than body size. Further analyses showed, however, that it was not possible to detect any evolutionary lag between canine size and body size, or between canine size dimorphism and body size dimorphism. Additional support for the notion of special selection on canine size consisted of allometric relationships in haplorhines between canine size and canine size dimorphism in males, as well as between canine size dimorphism and body size dimorphism. In conclusion, these analyses revealed that the effects of sexual selection on canine size are stronger than those on body size, perhaps indicating that canines are more important than body size in haplorhine male-male competition.     

The evolution of sexual size dimorphism in cottontail rabbits (Sylvilagus,Leporidae)

In mammals, ‘female‐biased’ sexual size dimorphism (SSD), in which females are larger than males, is uncommon. In the present study, we examined Sylvilagus, a purported case of female‐biased SSD, for evolutionary correlations among species between SSD, body‐size, and life‐history variables. We find that: (1) although most species are female‐biased, the degree and direction of SSD vary more than was previously recognized and (2) the degree of SSD decreases with increasing body size. Hence, Sylvilagus provides a new example, unusual for a female‐biased taxon, in which allometry for SSD is consistent with ‘Rensch's Rule’. As a corollary to Rensch's Rule, we observe that changes in SSD in Sylvilagus are typically associated with larger, more significant changes in males than females. Female‐biased SSD could be produced by selection for larger females, smaller males, or both. Although larger female size may be related to high fecundity and the extremely rapid fetal and neonatal growth in Sylvilagus, we find little evidence for a correlation between SSD and various fecundity‐related traits in among‐species comparisons. Smaller male size may confer greater reproductive success through greater mobility and reduced energetic requirements. We propose that a suite of traits (female dispersion, large male home ranges, reduced aggression, and a promiscuous mating system) has favoured smaller males and thus influenced the evolution of SSD in cottontails. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 141–156.     

Phylogeny suggests nondirectional and isometric evolution of sexual size dimorphism in argiopine spiders

Sexual dimorphism describes substantial differences between male and female phenotypes. In spiders, sexual dimorphism research almost exclusively focuses on size, and recent studies have recovered steady evolutionary size increases in females, and independent evolutionary size changes in males. Their discordance is due to negative allometric size patterns caused by different selection pressures on male and female sizes (converse Rensch's rule). Here, we investigated macroevolutionary patterns of sexual size dimorphism (SSD) in Argiopinae, a global lineage of orb‐weaving spiders with varying degrees of SSD. We devised a Bayesian and maximum‐likelihood molecular species‐level phylogeny, and then used it to reconstruct sex‐specific size evolution, to examine general hypotheses and different models of size evolution, to test for sexual size coevolution, and to examine allometric patterns of SSD. Our results, revealing ancestral moderate sizes and SSD, failed to reject the Brownian motion model, which suggests a nondirectional size evolution. Contrary to predictions, male and female sizes were phylogenetically correlated, and SSD evolution was isometric. We interpret these results to question the classical explanations of female‐biased SSD via fecundity, gravity, and differential mortality. In argiopines, SSD evolution may be driven by these or additional selection mechanisms, but perhaps at different phylogenetic scales.     

Sexual selection explains Rensch's rule of allometry for sexual size dimorphism

In 1950, Rensch first described that in groups of related species, sexual size dimorphism is more pronounced in larger species. This widespread and fundamental allometric relationship is now commonly referred to as 'Rensch's rule'. However, despite numerous recent studies, we still do not have a general explanation for this allometry. Here we report that patterns of allometry in over 5300 bird species demonstrate that Rensch's rule is driven by a correlated evolutionary change in females to directional sexual selection on males. First, in detailed multivariate analysis, the strength of sexual selection was, by far, the strongest predictor of allometry. This was found to be the case even after controlling for numerous potential confounding factors, such as overall size, degree of ornamentation, phylogenetic history and the range and degree of size dimorphism. Second, in groups where sexual selection is stronger in females, allometry consistently goes in the opposite direction to Rensch's rule. Taken together, these results provide the first clear solution to the long-standing evolutionary problem of allometry for sexual size dimorphism: sexual selection causes size dimorphism to correlate with species size.     

Local climate determines intra‐ and interspecific variation in sexual size dimorphism in mountain grasshopper communities

The climate is often evoked to explain broad‐scale clines of body size, yet its involvement in the processes that generate size inequality in the two sexes (sexual size dimorphism) remains elusive. Here, we analyse climatic clines of sexual size dimorphism along a wide elevation gradient (i) among grasshopper species in a phylogenetically controlled scenario and (ii) within species differing in distribution and cold tolerance, to highlight patterns generated at different time scales, mainly evolutionary (among species or higher taxa) and ontogenetic or microevolutionary (within species). At the interspecific level, grasshoppers were slightly smaller and less dimorphic at high elevations. These clines were associated with gradients of precipitation and sun exposure, which are likely indicators of other factors that directly exert selective pressures, such as resource availability and conditions for effective thermoregulation. Within species, we found a positive effect of temperature and a negative effect of elevation on body size, especially on condition‐dependent measures of body size (total body length rather than hind femur length) and in species inhabiting the highest elevations. In spite of a certain degree of species‐specific variation, females tended to adjust their body size more often than males, suggesting that body size in females can evolve faster among species and can be more plastic or dependent on nutritional conditions within species living in adverse climates. Natural selection on female body size may therefore prevail over sexual selection on male body size in alpine environments, and abiotic factors may trigger consistent phenotypic patterns across taxonomic scales.     

Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes

Females are larger than males in most invertebrate taxa, a phenomenon believed to result from the pressures exerted on female body size by size-dependent fecundity. Male-male competition, which can act on male body size, is not thought to play as important a role in the evolution of sexual size dimorphism in invertebrates as it apparently does in some vertebrate groups. Here, using a comparative approach, the relationship between sexual size dimorphism and adult sex ratio is examined across 46 natural populations (41 species) and 30 experimental populations (21 species) of parasitic nematodes. If male-male competition via physical contests is important, relative male size should increase as the sex ratio becomes less female-biased. This is exactly what was found in the analyses, where residuals of male size regressed on female size were used as measures of sexual size dimorphism. This result was independent of any phylogenetic influences, and was obtained for both natural and experimental nematode populations. In addition, there was no evidence of any Allometric relationship between male and female body size. The average ratio of male size to female size was roughly constant across all species and independent of body size. The results are consistent with a role for male-male competition in explaining specific deviations from the average ratio of male to female body size, suggesting a significant role for sexual selection in the evolution of nematode body sizes.     

Interrelations of global macroecological patterns in wing and thorax size,sexual size dimorphism,and range size of the Drosophilidae

Support for macroecological rules in insects is mixed, with potential confounding interrelations between patterns rarely studied. We here investigate global patterns in body and wing size, sexual size dimorphism and range size in common fruit flies (Diptera: Drosophilidae) and explore potential interrelations and the predictive power of Allen's, Bergmann's, Rensch's and Rapoport's rules. We found that thorax length (r² = 0.05) and wing size (r² = 0.09) increased with latitude, supporting Bergmann's rule. Contrary to patterns often found in endothermic vertebrates, relative wing size increased towards the poles (r² = 0.12), a pattern against Allen's rule, which we attribute to selection for increased flight capacity in the cold. Sexual size dimorphism decreased with size, evincing Rensch's rule across the family (r² = 0.14). Yet, this pattern was largely driven by the virilis–repleta radiation. Finally, range size did not correlate with latitude, although a positive relationship was present in a subset of the species investigated, providing no convincing evidence for Rapoport's rule. We further found little support for confounding interrelations between body size, wing loading and range size in this taxon. Nevertheless, we demonstrate that studying several traits simultaneously at minimum permits better interpretation in case of multiple, potentially conflicting trends or hypotheses concerning the macroecology of insects.     

Variation in body size and sexual size dimorphism in the most widely ranging lizard: testing the effects of reproductive mode and climate

Reproductive mode, ancestry, and climate are hypothesized to determine body size variation in reptiles but their effects have rarely been estimated simultaneously, especially at the intraspecific level. The common lizard (Zootoca vivipara) occupies almost the entire Northern Eurasia and includes viviparous and oviparous lineages, thus representing an excellent model for such studies. Using body length data for >10,000 individuals from 72 geographically distinct populations over the species' range, we analyzed how sex‐specific adult body size and sexual size dimorphism (SSD) is associated with reproductive mode, lineage identity, and several climatic variables. Variation in male size was low and poorly explained by our predictors. In contrast, female size and SSD varied considerably, demonstrating significant effects of reproductive mode and particularly seasonality. Populations of the western oviparous lineage (northern Spain, south‐western France) exhibited a smaller female size and less female‐biased SSD than those of the western viviparous (France to Eastern Europe) and the eastern viviparous (Eastern Europe to Far East) lineages; this pattern persisted even after controlling for climatic effects. The phenotypic response to seasonality was complex: across the lineages, as well as within the eastern viviparous lineage, female size and SSD increase with increasing seasonality, whereas the western viviparous lineage followed the opposing trends. Altogether, viviparous populations seem to follow a saw‐tooth geographic cline, which might reflect the nonmonotonic relationship of body size at maturity in females with the length of activity season. This relationship is predicted to arise in perennial ectotherms as a response to environmental constraints caused by seasonality of growth and reproduction. The SSD allometry followed the converse of Rensch's rule, a rare pattern for amniotes. Our results provide the first evidence of opposing body size—climate relationships in intraspecific units.     

Sexual size dimorphism in domestic goats,sheep, and their wild relatives

Sexual size dimorphism (SSD) is a widespread phenomenon in different animal taxa, including the subfamily of goats and sheep (Caprinae), which belongs to the most dimorphic mammalian groups. Rensch's rule describes the pattern of SSD, claiming that larger species generally exhibits higher male to female body size ratio. Agreement with Rensch's rule is manifested by slope of the allometric relationship between male and female body size exceeding one. To test this rule, we analysed the data available in the literature on adult body mass of males and females in domestic goat and sheep breeds (169 and 303, respectively) and 37 wild species/subspecies of the subfamily Caprinae. According to the current phylogenetical hypotheses, there are six distinct monophyletic groups with different levels of SSD (expressed as M/F): (1) wild goats (1.83); (2) wild sheep (1.67); (3) non‐European chamoises, including Ovibos moschatus (1.18); (4) European chamoises (1.27); (5) Budorcas taxicolor (1.01); and (6) Pantholops hodgsonii (1.65). Domestication has led to a remarkable decline in SSD of both domestic goats (1.36) and sheep (1.41). The highest regression slope of the relationship between male and female body size is that estimated for wild goats (1.32), followed by wild sheep (1.24), non‐European chamoises (1.14), domestic sheep (1.13), and domestic goats (1.10). Nevertheless, only the last two values are statistically different from one and thus corroborate Rensch's rule. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 872–883.     

Ecological drivers of body size evolution and sexual size dimorphism in short‐horned grasshoppers (Orthoptera: Acrididae)

Sexual size dimorphism (SSD) is widespread and variable in nature. Although female‐biased SSD predominates among insects, the proximate ecological and evolutionary factors promoting this phenomenon remain largely unstudied. Here, we employ modern phylogenetic comparative methods on eight subfamilies of Iberian grasshoppers (85 species) to examine the validity of different models of evolution of body size and SSD and explore how they are shaped by a suite of ecological variables (habitat specialization, substrate use, altitude) and/or constrained by different evolutionary pressures (female fecundity, strength of sexual selection, length of the breeding season). Body size disparity primarily accumulated late in the history of the group and did not follow a Brownian motion pattern, indicating the existence of directional evolution for this trait. We found support for the converse of Rensch's rule (i.e. females are proportionally bigger than males in large species) across all taxa but not within the two most speciose subfamilies (Gomphocerinae and Oedipodinae), which showed an isometric pattern. Our results do not provide support for the fecundity or sexual selection hypotheses, and we did not find evidence for significant effects of habitat use. Contrary to that expected, we found that species with narrower reproductive window are less dimorphic in size than those that exhibit a longer breeding cycle, suggesting that male protandry cannot solely account for the evolution of female‐biased SSD in Orthoptera. Our study highlights the need to consider alternatives to the classical evolutionary hypotheses when trying to explain why in certain insect groups males remain small.     

Rensch's rule, Bergmann's effect and adult sexual dimorphism in wild monogamous owl monkeys (Aotus azarai) of Argentina

Some monogamous primates are characterized by biparental care, territoriality, and a reduced level of physical dimorphism. In others, the relationship between those behavioral patterns and dimorphism is less clear. I tested Bergmann's and Rensch's rules using Aotus spp. body mass data and I characterized the extent of sexual dimorphism in body mass, dental and physical measurements in a socially monogamous owl monkey population (n = 91 adults) from the Argentinean Gran Chaco. A. azarai azarai from the Argentinean Chaco is larger than the more tropical owl monkey species (r = 0.7, N = 6 species), but there is no apparent increase in sexual dimorphism with increased body mass. The body masses of adult male and female A. a. azarai were remarkably similar (Mean = 1.26 kg); there were no marked sex differences in most skeletal measurements, but males had higher and wider upper and lower canines than did females. Body mass and neck circumference were positively and strongly related (r = 0.533, n = 52), and the body mass of adults was not a reliable indicator of their age (r = 0.03, n = 10). The data illustrate the complexities inherent in examining and summarizing within population variation in skeletal and nonskeletal measurements and contribute to a better understanding of the relationships between monogamous behavioral patterns and sexual dimorphism.     

The relationship between sexual size dimorphism and habitat use in Greater Antillean Anolis lizards

Abstract.— Sexual size dimorphism (SSD) is the evolutionary result of selection operating differently on the body sizes of males and females. Anolis lizard species of the Greater Antilles have been classified into ecomorph classes, largely on the basis of their structural habitat (perch height and diameter). We show that the major ecomorph classes differ in degree of SSD. At least two SSD classes are supported: high SSD (trunk-crown, trunk-ground) and low SSD (trunk, crown-giant, grass-bush, twig). Differences cannot be attributed to an allometric increase of SSD with body size or to a phylogenetic effect. A third explanation, that selective pressures on male and/or female body size vary among habitat types, is examined by evaluating expectations from the major relevant kinds of selective pressures. Although no one kind of selective pressure produces expectations consistent with all of the information, competition with respect to structural habitat and sexual selection pressures are more likely possibilities than competition with respect to prey size or optimal feeding pressures. The existence of habitat-specific sexual dimorphism suggests that adaptation of Anolis species to their environment is more complex than previously appreciated.     

Sexual selection explains sex-specific growth plasticity and positive allometry for sexual size dimorphism in a reef fish

In 1950, Rensch noted that in clades where males are the larger sex, sexual size dimorphism (SSD) tends to be more pronounced in larger species. This fundamental allometric relationship is now known as ‘Rensch''s rule’. While most researchers attribute Rensch''s rule to sexual selection for male size, experimental evidence is lacking. Here, we suggest that ultimate hypotheses for Rensch''s rule should also apply to groups of individuals and that individual trait plasticity can be used to test those hypotheses experimentally. Specifically, we show that in the sex-changing fish Parapercis cylindrica, larger males have larger harems with larger females, and that SSD increases with harem size. Thus, sexual selection for male body size is the ultimate cause of sexual size allometry. In addition, we experimentally illustrate a positive relationship between polygyny potential and individual growth rate during sex change from female to male. Thus, sexual selection is the ultimate cause of variation in growth rate, and variation in growth rate is the proximate cause of sexual size allometry. Taken together, our results provide compelling evidence in support of the sexual selection hypothesis for Rensch''s rule and highlight the potential importance of individual growth modification in the shaping of morphological patterns in Nature.     

Macroevolutionary pattern of sexual size dimorphism in geckos corresponds to intraspecific temperature‐induced variation

Many animal lineages exhibit allometry in sexual size dimorphism (SSD), known as ‘Rensch’s rule’. When applied to the interspecific level, this rule states that males are more evolutionary plastic in body size than females and that male‐biased SSD increases with body size. One of the explanations for the occurrence of Rensch’s rule is the differential‐plasticity hypothesis assuming that higher evolutionary plasticity in males is a consequence of larger sensitivity of male growth to environmental cues. We have confirmed the pattern consistent with Rensch’s rule among species of the gecko genus Paroedura and followed the ontogeny of SSD at three constant temperatures in a male‐larger species (Paroedura picta). In this species, males exhibited larger temperature‐induced phenotypic plasticity in final body size than females, and body size and SSD correlated across temperatures. This result supports the differential‐plasticity hypothesis and points to the role phenotypic plasticity plays in generating of evolutionary novelties.     

Latitudinal variation in sexual dimorphism in life‐history traits of a freshwater fish

Sexual dimorphism is common across the animal kingdom, but the contribution of environmental factors shaping differences between the sexes remains controversial. In ectotherms, life‐history traits are known to correlate with latitude, but sex‐specific responses are not well understood. We analyzed life‐history trait variation between the sexes of European perch (Perca fluviatilis L.), a common freshwater fish displaying larger female size, by employing a wide latitudinal gradient. We expected to find sex‐dependent latitudinal variation in life‐history variables: length at age, length increment, and size at maturity, with females showing consistently higher values than males at all latitudes. We further anticipated that this gender difference would progressively decrease with the increasingly harsh environmental conditions toward higher latitude. We hypothesized that growth and length increment would decrease and size/age at maturity would increase at higher latitudes. Our results confirmed female‐biased sexual size dimorphism at all latitudes and the magnitude of sexual dimorphism diminished with increase in latitude. Growth of both sexes decreased with increase in latitude, and the female latitudinal clines were steeper than those of males. Hence, we challenge two predominant ecological rules (Rensch's and Bergmann's rules) that describe common large‐scale patterns of body size variation. Our data demonstrate that these two rules are not universally applicable in ectotherms or female‐biased species. Our study highlights the importance of sex‐specific differences in life‐history traits along a latitudinal gradient, with evident implications for a wide range of studies from individual to ecosystems level.     

Macroevolutionary patterns of sexual size dimorphism in copepods

Major theories compete to explain the macroevolutionary trends observed in sexual size dimorphism (SSD) in animals. Quantitative genetic theory suggests that the sex under historically stronger directional selection will exhibit greater interspecific variance in size, with covariation between allometric slopes (male to female size) and the strength of SSD across clades. Rensch''s rule (RR) also suggests a correlation, but one in which males are always the more size variant sex. Examining free-living pelagic and parasitic Copepoda, we test these competing predictions. Females are commonly the larger sex in copepod species. Comparing clades that vary by four orders of magnitude in their degree of dimorphism, we show that isometry is widespread. As such we find no support for either RR or for covariation between allometry and SSD. Our results suggest that selection on both sexes has been equally important. We next test the prediction that variation in the degree of SSD is related to the adult sex ratio. As males become relatively less abundant, it has been hypothesized that this will lead to a reduction in both inter-male competition and male size. However, the lack of such a correlation across diverse free-living pelagic families of copepods provides no support for this hypothesis. By comparison, in sea lice of the family Caligidae, there is some qualitative support of the hypothesis, males may suffer elevated mortality when they leave the host and rove for sedentary females, and their female-biased SSD is greater than in many free-living families. However, other parasitic copepods which do not appear to have obvious differences in sex-based mate searching risks also show similar or even more extreme SSD, therefore suggesting other factors can drive the observed extremes.     

Latitudinal variation in cranial dimorphism in Macaca fascicularis

This study examines latitudinal and insular variation in the expression of sexual dimorphism in cranial length in three geographical groupings of Macaca fascicularis. In addition, the relationship between cranial length dimorphism (CLD) and sex‐specific size is examined. The results of the study identified a significant relationship between CLD and latitude for only one of the three geographic groupings. Sex‐specific relationships between cranial length and CLD were detected. The pattern of these relationships varied by geographic grouping. This study is important because it demonstrates that despite very similar levels of CLD in a single primate species, there exists important geographic variability in the correlates of that dimorphism. I suggest that geographically varying ecological factors may influence sex‐specific natural selection and the intensity of CLD in M. fascicularis. Gaining a better understanding of this geographical variability will require that future research examines morphological variation, including CLD, within its corresponding ecological and social contexts. Such research should be comparative, and incorporate multiple geographically separated populations with disparate environmental settings. Am. J. Primatol. 72:152–160, 2010. © 2009 Wiley‐Liss, Inc.     

Role of sexual and natural selection in evolution of body size and shape: a phylogenetic study of morphological radiation in grouse

We use standardized independent contrasts (SICs) to elucidate the effect of ecology and mating systems on morphological radiation in grouse. The analysis of SICs for 38 skeletal measurements from 20 taxa, showed that changes in mating system had a significant effect on body size of both sexes. Sexual size dimorphism in grouse is consistent with Rensch's rule; the slope of the regression of male vs. female size SICs was 1.4, significantly >1. Changes in habitat were associated with accelerated rates of evolution of body proportions. SICs for male and female scores of size independent factors were directly proportional to each other (slope = 1), indicating extreme similarities between male and female ecology. Females, however, were better adapted to longer, more energy efficient flight than males. Size independent morphological differences among grouse are adaptive and are related to the differences in habitat and foraging behaviour among the species.     

Sexual dimorphism in cranial shape and size in geomyoid rodents: multivariate and evolutionary perspectives

Geomyoid rodents provide a great study system for the analysis of sexual dimorphism. They are polygynic and many inhabit harsh arid environments thought to promote sexual dimorphism. In fact, there has been extensive work published on the sexual size dimorphism of individual populations and species within this rodent clade. However, little work has been undertaken to assess the evolutionary patterns and processes associated with this sexual dimorphism. We use multivariate analyses of cranial measurements in a phylogenetic framework to determine the distribution of size and shape dimorphism among geomyoids and test for Rensch’s rule. Our results suggest that sexual dimorphism is more common in geomyids than heteromyids, but it is not in fact universal. There is evidence for variation in sexual dimorphism across populations. Additionally, in many taxa, geographic variation appears to overwhelm existing sexual dimorphism. We find support for the repeated independent evolution of shape and size dimorphism across geomyoid taxa, but we do not find support for an association between size and shape dimorphism. There is no evidence for Rensch’s rule in geomyoids, whether at the superfamily or family level. Together, our findings suggest that there is no single explanation for the evolution of sexual dimorphism in geomyoids and that, instead, it is the product of numerous evolutionary events. Future studies incorporating phylogenetic relationships will be necessary to paint a more complete picture of the evolution of sexual dimorphism in geomyoids.