Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Sexual dimorphism can evolve when males and females differ in phenotypic optima. Genetic constraints can, however, limit the evolution of sexual dimorphism. One possible constraint is derived from alleles expressed in both sexes. Because males and females share most of their genome, shared alleles with different fitness effects between sexes are faced with intralocus sexual conflict. Another potential constraint is derived from genetic correlations between developmental stages. Sexually dimorphic traits are often favoured at adult stages, but selected against as juvenile, so developmental decoupling of traits between ontogenetic stages may be necessary for the evolution of sexual dimorphism in adults. Resolving intralocus conflicts between sexes and ages is therefore a key to the evolution of age‐specific expression of sexual dimorphism. We investigated the genetic architecture of divergence in the ontogeny of sexual dimorphism between two populations of the Japanese medaka (Oryzias latipes) that differ in the magnitude of dimorphism in anal and dorsal fin length. Quantitative trait loci (QTL) mapping revealed that few QTL had consistent effects throughout ontogenetic stages and the majority of QTL change the sizes and directions of effects on fin growth rates during ontogeny. We also found that most QTL were sex‐specific, suggesting that intralocus sexual conflict is almost resolved. Our results indicate that sex‐ and age‐specific QTL enable the populations to achieve optimal developmental trajectories of sexually dimorphic traits in response to complex natural and sexual selection.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation

An evolutionary response to selection requires genetic variation; however, even if it exists, then the genetic details of the variation can constrain adaptation. In the simplest case, unlinked loci and uncorrelated phenotypes respond directly to multivariate selection and permit unrestricted paths to adaptive peaks. By contrast, ‘antagonistic’ pleiotropic loci may constrain adaptation by affecting variation of many traits and limiting the direction of trait correlations to vectors that are not favoured by selection. However, certain pleiotropic configurations may improve the conditions for adaptive evolution. Here, we present evidence that the Arabidopsis thaliana gene FRI (FRIGIDA) exhibits ‘adaptive’ pleiotropy, producing trait correlations along an axis that results in two adaptive strategies. Derived, low expression FRI alleles confer a ‘drought escape’ strategy owing to fast growth, low water use efficiency and early flowering. By contrast, a dehydration avoidance strategy is conferred by the ancestral phenotype of late flowering, slow growth and efficient water use during photosynthesis. The dehydration avoidant phenotype was recovered when genotypes with null FRI alleles were transformed with functional alleles. Our findings indicate that the well-documented effects of FRI on phenology result from differences in physiology, not only a simple developmental switch.     

Life history,sexual dimorphism and ‘ornamental’ feathers in the mesozoic bird Confuciusornis sanctus

The life history of Confuciusornis sanctus is controversial. Recently, the species’ body size spectrum was claimed to contradict osteohistological evidence for a rapid, bird-like development. Moreover, sexual size dimorphism was rejected as an explanation for the observed bimodal size distribution since the presence of elongated rectrices, an assumed ‘male’ trait, was uncorrelated with size. However, this interpretation (i) fails to explain the size spectrum of C. sanctus which is trimodal rather than bimodal, (ii) requires implausible neonate masses and (iii) is not supported by analogy with sexual dimorphisms in modern birds, in which elongated central rectrices are mostly sex-independent. Available information on C. sanctus is readily reconciled if we assume a bird-like life history, as well as a pronounced sexual size dimorphism and sexually isomorphic extravagant feathers as frequently observed in extant species.     

Evidence for the secondary sexual development of the anal fin in female kokanee salmon Oncorhynchus nerka

This study examines whether the anal fin undergoes secondary sexual development similar to other reproductive traits in salmonids. This hypothesis was tested by comparing the anal‐fin size of female kokanee salmon Oncorhynchus nerka that were in the early and late stages of sexual development. Females in an advanced stage of maturation had significantly larger anal fins relative to females in an early state of maturation (+4–7%), indicating that the anal fin undergoes secondary sexual development. The magnitude of this secondary growth was comparable with snout length (+9–10%), which is known to undergo secondary sexual development in female salmonids. When morphological trait dimensions were compared between the sexes, the anal fin was the only morphological trait found to have a female‐biased sexual size dimorphism. This is the first study to show that the anal fin of female salmonids undergoes secondary sexual development.     

Sexual dimorphism in the quantitative-genetic architecture of floral, leaf, and allocation traits in Silene latifolia

Many species exhibit sexual dimorphism in a variety of characters, and the underlying genetic architecture of dimorphism potentially involves sex-specific differences in the additive-genetic variance-covariance matrix (G) of dimorphic traits. We investigated the quantitative-genetic structure of dimorphic traits in the dioecious plant Silene latifolia by estimating G (including within-sex matrices, G(m), G(f), and the between-sex variance-covariance matrix, B), and the phenotypic variance-covariance matrix (P) for seven traits. Flower number was the most sexually dimorphic trait, and was significantly genetically correlated with all traits within each sex. Negative genetic correlations between flower size and number suggested a genetic trade-off in investment, but positive environmental correlations between the same traits resulted in no physical evidence for a trade-off in the phenotype. Between-sex genetic covariances for homologous traits were always greater than 0 but smaller than 1, showing that some, but not all, of the variation in traits is caused by genes or alleles with sex-limited expression. Using common principal-components analysis (CPCA), a maximum-likelihood (ML) estimation approach, and element-by-element comparison to compare matrices, we found that G(m) and G(f) differed significantly in eigenstructure because of dissimilarity in covariances involving leaf traits, suggesting the presence of variation in sex-limited genes with pleiotropic effects and/or linkage between sex-limited loci. The sex-specific structure of G is expected to cause differences in the correlated responses to selection within each sex, promoting the further evolution and maintenance of dimorphism.     

Odour cues from suitors’ nests determine mating success in a fish

Animals use a range of sensory cues for finding food, avoiding predators and choosing mates. In this regard, the aquatic environment is particularly suitable for the use of olfactory and other chemical cues. Nevertheless, mate choice research, even on aquatic organisms, has focused on visual signals, while chemical cues relevant in sexual selection have been assumed to be ‘intrinsic’ excretions of mate candidates. Here, using the sand goby Pomatoschistus minutus, a small fish with paternal egg care, we investigated the possibility that ‘extrinsic’ chemical cues in the males’ nests could also have a significant contribution to mating success. We found that females strongly avoided laying eggs into nests subject to the odour of Saprolegnia water moulds (an egg infection) and that this effect was independent of the females’ initial, visually based preference for males. To the best of our knowledge, this is the first study to show that chemical cues related to parental failure can play a large role in sexual selection.     

Sexual antagonism for resistance and tolerance to infection in Drosophila melanogaster

A critical task in evolutionary genetics is to explain the persistence of heritable variation in fitness-related traits such as immunity. Ecological factors can maintain genetic variation in immunity, but less is known about the role of other factors, such as antagonistic pleiotropy, on immunity. Sexually dimorphic immunity—with females often being more immune-competent—may maintain variation in immunity in dioecious populations. Most eco-immunological studies assess host resistance to parasites rather than the host''s ability to maintain fitness during infection (tolerance). Distinguishing between resistance and tolerance is important as they are thought to have markedly different evolutionary and epidemiological outcomes. Few studies have investigated tolerance in animals, and the extent of sexual dimorphism in tolerance is unknown. Using males and females from 50 Drosophila melanogaster genotypes, we investigated possible sources of genetic variation for immunity by assessing both resistance and tolerance to the common bacterial pathogen Pseudomonas aeruginosa. We found evidence of sexual dimorphism and sexual antagonism for resistance and tolerance, and a trade-off between the two traits. Our findings suggest that antagonistic pleiotropy may be a major contributor to variation in immunity, with implications for host–parasite coevolution.     

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.     

Social context-dependent modification of courtship behaviour in Drosophila prolongata

Induction of alternative mating tactics by surrounding conditions, such as the presence of conspecific males, is observed in many animal species. Satellite behaviour is a remarkable example in which parasitic males exploit the reproductive investment by other males. Despite the abundance of parasitic mating tactics, however, few examples are known in which males alter courtship behaviour as a counter tactic against parasitic rivals. The fruit fly Drosophila prolongata shows prominent sexual dimorphism in the forelegs. When courting females, males of D. prolongata perform ‘leg vibration’, in which a male vibrates the female''s body with his enlarged forelegs. In this study, we found that leg vibration increased female receptivity, but it also raised a risk of interception of the female by rival males. Consequently, in the presence of rivals, males of D. prolongata shifted their courtship behaviour from leg vibration to ‘rubbing’, which was less vulnerable to interference by rival males. These results demonstrated that the males of D. prolongata adjust their courtship behaviour to circumvent the social context-dependent risk of leg vibration.     

Effects of Infection by Belonolaimus longicaudatus on Rooting Dynamics among St. Augustinegrass and Bermudagrass Genotypes

Understanding rooting dynamics using the minirhizotron technique is useful for cultivar selection and to quantify nematode damage to roots. A 2-yr microplot study including five bermudagrass (‘Tifway’, Belonolaimus longicaudatus susceptible; two commercial cultivars [TifSport and Celebration] and two genotypes [‘BA132’ and ‘PI 291590’], which have been reported to be tolerant to B. longicaudatus) and two St. Augustinegrass (‘FX 313’, susceptible, and ‘Floratam’ that was reported as tolerant to B. longicaudatus) genotypes in a 5 x 2 and 2 x 2 factorial design with four replications, respectively, was initiated in 2012. Two treatments included were uninoculated and B. longicaudatus inoculated. In situ root images were captured each month using a minirhizotron camera system from April to September of 2013 and 2014. Mixed models analysis and comparison of least squares means indicated significant differences in root parameters studied across the genotypes and soil depths of both grass species. ‘Celebration’, ‘TifSport’ and ‘PI 291590’ bermudagrass, and ‘Floratam’ St. Augustinegrass had significantly different root parameters compared to the corresponding susceptible genotypes (P ≤ 0.05). Only ‘TifSport’ had no significant root loss when infested with B. longicaudatus compared to non-infested. ‘Celebration’ and ‘PI 291590’ had significant root loss but retained significantly greater root densities than ‘Tifway’ in B. longicaudatus-infested conditions (P ≤ 0.05). Root lengths were greater at the 0 to 5 cm depth followed by 5 to 10 and 10 to 15 cm of vertical soil depth for both grass species (P ≤ 0.05). ‘Celebration’, ‘TifSport’, and ‘PI 291590’ had better root vigor against B. longicaudatus compared to Tifway.     

A multivariate view of the evolution of sexual dimorphism

Sexual differences are often dramatic and widespread across taxa. Their extravagance and ubiquity can be puzzling because the common underlying genome of males and females is expected to impede rather than foster phenotypic divergence. Widespread dimorphism, despite a shared genome, may be more readily explained by considering the multivariate, rather than univariate, framework governing the evolution of sexual dimorphism. In the univariate formulation, differences in genetic variances and a low intersexual genetic correlation () can facilitate the evolution of sexual dimorphism. However, studies that have analysed sex‐specific differences in heritabilities or genetic variances do not always find significant differences. Furthermore, many of the reported estimates of are very high and positive. When monomorphic heritabilities and a high are present together, the evolution of sexual dimorphism on a trait‐by‐trait basis is severely constrained. By contrast, the multivariate formulation has greater generality and more flexibility. Although the number of multivariate sexual dimorphism studies is low, almost all support sex‐specific differences in the G (variance‐covariance) matrix; G matrices can differ with respect to size and/or orientation, affecting the response to selection differently between the sexes. Second, whereas positive values of the univariate quantity only hinder positive changes in sexual dimorphism, positive covariances in the intersexual covariance B matrix can either help or hinder. Similarly, the handful of studies reporting B matrices indicate that it is often asymmetric, so that B can affect the evolution of single traits differently between the sexes. Multivariate approaches typically demonstrate that genetic covariances among traits can strongly constrain trait evolution when compared with univariate approaches. By contrast, in the evolution of sexual dimorphism, a multivariate view potentially reveals more opportunities for sexual dimorphism to evolve by considering the effect sex‐specific selection has on sex‐specific G matrices and an asymmetric B matrix.     

Peak shifts and extinction under sex-specific selection

A well-known property of sexual selection combined with a cross-sex genetic correlation (r_mf) is that it can facilitate a peak shift on the adaptive landscape. How do these diversifying effects of sexual selection + r_mf balance with the constraints imposed by such sexual antagonism, to affect the macroevolution of sexual dimorphism? Here, I extend existing quantitative genetic models of evolution on complex adaptive landscapes. Beyond recovering classical predictions for the conditions promoting a peak shift, I show that when r_mf is moderate to strong, relatively weak sexual selection is required to induce a peak shift in males only. Increasing the strength of sexual selection leads to a sexually concordant peak shift, suggesting that macroevolutionary rates of sexual dimorphism may be largely decoupled from the strength of within-population sexual selection. Accounting explicitly for demography further reveals that sex-specific peak shifts may be more likely to be successful than concordant shifts in the face of extinction, especially when natural selection is strong. An overarching conclusion is that macroevolutionary patterns of sexual dimorphism are unlikely to be readily explained by within-population estimates of selection or constraint alone.     

Adult sex ratio,sexual dimorphism and sexual selection in a Mesozoic reptile

The evolutionary history of sexual selection in the geologic past is poorly documented based on quantification, largely because of difficulty in sexing fossil specimens. Even such essential ecological parameters as adult sex ratio (ASR) and sexual size dimorphism (SSD) are rarely quantified, despite their implications for sexual selection. To enable their estimation, we propose a method for unbiased sex identification based on sexual shape dimorphism, using size-independent principal components of phenotypic data. We applied the method to test sexual selection in Keichousaurus hui, a Middle Triassic (about 237 Ma) sauropterygian with an unusually large sample size for a fossil reptile. Keichousaurus hui exhibited SSD biased towards males, as in the majority of extant reptiles, to a minor degree (sexual dimorphism index −0.087). The ASR is about 60% females, suggesting higher mortality of males over females. Both values support sexual selection of males in this species. The method may be applied to other fossil species. We also used the Gompertz allometric equation to study the sexual shape dimorphism of K. hui and found that two sexes had largely homogeneous phenotypes at birth except in the humeral width, contrary to previous suggestions derived from the standard allometric equation.     

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Sexual dimorphism is typically a result of strong sexual selection on male traits used in male–male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females—but not males—were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela—the primary antagonistic weapon in snapping shrimps—increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female–female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.     

Effects of laboratory colonization on Bactrocera dorsalis (Diptera,Tephritidae) mating behaviour: ‘what a difference a year makes’

Laboratory-reared insects are widely known to have significantly reduced genetic diversity in comparison to wild populations; however, subtle behavioural changes between laboratory-adapted and wild or ‘wildish’ (i.e., within one or very few generations of field collected material) populations are less well understood. Quantifying alterations in behaviour, particularly sexual, in laboratory-adapted insects is important for mass-reared insects for use in pest management strategies, especially those that have a sterile insect technique component. We report subtle changes in sexual behaviour between ‘wildish’ Bactrocera dorsalis flies (F1 and F2) from central and southern Thailand and the same colonies 12 months later when at six generations from wild. Mating compatibility tests were undertaken under standardised semi-natural conditions, with number of homo/heterotypic couples and mating location in field cages analysed via compatibility indices. Central and southern populations of Bactrocera dorsalis displayed positive assortative mating in the 2010 trials but mated randomly in the 2011 trials. ‘Wildish’ southern Thailand males mated significantly earlier than central Thailand males in 2010; this difference was considerably reduced in 2011, yet homotypic couples from southern Thailand still formed significantly earlier than all other couple combinations. There was no significant difference in couple location in 2010; however, couple location significantly differed among pair types in 2011 with those involving southern Thailand females occurring significantly more often on the tree relative to those with central Thailand females. Relative participation also changed with time, with more southern Thailand females forming couples relative to central Thailand females in 2010; this difference was considerably decreased by 2011. These results reveal how subtle changes in sexual behaviour, as driven by laboratory rearing conditions, may significantly influence mating behaviour between laboratory-adapted and recently colonised tephritid fruit flies over a relatively short period of time.     

Evidence for the circadian gene period as a proximate mechanism of protandry in a pollinating fig wasp

Protandry in insects is the tendency for adult males to emerge before females and usually results from intra-sexual selection. However, the genetic basis of this common phenomenon is poorly understood. Pollinating fig wasp (Agaonidae) larvae develop in galled flowers within the enclosed inflorescences (‘figs’) of fig trees. Upon emergence, males locate and mate with the still galled females. After mating, males release females from their galls to enable dispersal. Females cannot exit galls or disperse from a fig without male assistance. We sampled male and female Ceratosolen solmsi (the pollinator of Ficus hispida) every 3 h over a 24 h emergence period, and then measured the expression of five circadian genes: period (per), clock (clk), cycle (cyc), pigment-dispersing factor (pdf) and clockwork orange (cwo). We found significant male-biased sexual dimorphism in the expression of all five genes. per showed the greatest divergence between the sexes and was the only gene rhythmically expressed. Expression of per correlated closely with emergence rates at specific time intervals in both male and female wasps. We suggest that this rhythmical expression of per may be a proximate mechanism of protandry in this species.     

Sexual dimorphism and allometry of external morphology in Oreochromis mossambicus

Sexual dimorphism in growth of conventional morphometric characters was investigated in juveniles and young adults (size range: 31 to 91 mm) of Oreochromis mossambicus . A closely associated set of traits was identified that shows sexually dimorphic growth, which was positively allometric in the males. These traits correspond to two different morphological complexes: jaw structure and anal/dorsal fins. The best sex discriminators among this set of traits were premaxilla width, anal fin height and snout length. These findings may be explained in terms of intra– and inter–sexual selection acting together and favouring males with strong and large mouths and high dorsal and anal fins, traits that are important in agonistic displays (jaw and fins), fighting and nest digging (jaw).     

A Middle Triassic thoracopterid from China highlights the evolutionary origin of overwater gliding in early ray-finned fishes

Gliding adaptations in thoracopterid flying fishes represent a remarkable case of convergent evolution of overwater gliding strategy with modern exocoetid flying fishes, but the evolutionary origin of this strategy was poorly known in the thoracopterids because of lack of transitional forms. Until recently, all thoracopterids, from the Late Triassic of Austria and Italy and the Middle Triassic of South China, were highly specialized ‘four-winged’ gliders in having wing-like paired fins and an asymmetrical caudal fin with the lower caudal lobe notably larger than the upper lobe. Here, we show that the new genus Wushaichthys and the previously alleged ‘peltopleurid’ Peripeltopleurus, from the Middle Triassic (Ladinian, 235–242 Ma) of South China and near the Ladinian/Anisian boundary of southern Switzerland and northern Italy, respectively, represent the most primitive and oldest known thoracopterids. Wushaichthys, the most basal thoracopterid, shows certain derived features of this group in the skull. Peripeltopleurus shows a condition intermediate between Wushaichthys and Thoracopterus in having a slightly asymmetrical caudal fin but still lacking wing-like paired fins. Phylogenetic studies suggest that the evolution of overwater gliding of thoracopterids was gradual in nature; a four-stage adaption following the ‘cranial specialization–asymmetrical caudal fin–enlarged paired fins–scale reduction’ sequence has been recognized in thoracopterid evolution. Moreover, Wushaichthys and Peripeltopleurus bear hooklets on the anal fin of supposed males, resembling those of modern viviparious teleosts. Early thoracopterids probably had evolved a live-bearing reproductive strategy.     

Sexual dichromatism in frogs: natural selection, sexual selection and unexpected diversity

Sexual dichromatism, a form of sexual dimorphism in which males and females differ in colour, is widespread in animals but has been predominantly studied in birds, fishes and butterflies. Moreover, although there are several proposed evolutionary mechanisms for sexual dichromatism in vertebrates, few studies have examined this phenomenon outside the context of sexual selection. Here, we describe unexpectedly high diversity of sexual dichromatism in frogs and create a comparative framework to guide future analyses of the evolution of these sexual colour differences. We review what is known about evolution of colour dimorphism in frogs, highlight alternative mechanisms that may contribute to the evolution of sexual colour differences, and compare them to mechanisms active in other major groups of vertebrates. In frogs, sexual dichromatism can be dynamic (temporary colour change in males) or ontogenetic (permanent colour change in males or females). The degree and the duration of sexual colour differences vary greatly across lineages, and we do not detect phylogenetic signal in the distribution of this trait, therefore frogs provide an opportunity to investigate the roles of natural and sexual selection across multiple independent derivations of sexual dichromatism.