Field estimates of parentage reveal sexually antagonistic selection on body size in a population of Anolis lizards

Sexual dimorphism evolves when selection favors different phenotypic optima between the sexes. Such sexually antagonistic selection creates intralocus sexual conflict when traits are genetically correlated between the sexes and have sex‐specific optima. Brown anoles are highly sexually dimorphic: Males are on average 30% longer than females and 150% heavier in our study population. Viability selection on body size is known to be sexually antagonistic, and directional selection favors large male size whereas stabilizing selection constrains females to remain small. We build on previous studies of viability selection by measuring sexually antagonistic selection using reproductive components of fitness over three generations in a natural population of brown anoles. We estimated the number of offspring produced by an individual that survived to sexual maturity (termed RS^V), a measure of individual fitness that includes aspects of both individual reproductive success and offspring survival. We found directional selection on male body size, consistent with previous studies of viability selection. However, selection on female body size varied among years, and included periods of positive directional selection, quadratic stabilizing selection, and no selection. Selection acts differently in the sexes based on both survival and reproduction and sexual conflict appears to be a persistent force in this species.     

Characterizing selection in black‐throated blue warblers using a sexual network approach

Our understanding of trait evolution is built upon studies that examine the correlation between traits and fitness, most of which implicitly assume all individuals experience similar selective environments. However, accounting for differences in selective pressures, such as variation in the social environment, can advance our understanding of how selection shapes individual traits and subsequent fitness. In this study, we test whether variation in the social environment affects selection on individual phenotype. We apply a new sexual network framework to quantify each male's social environment as the mean body size of his primary competitors. We test for direct and social selection on male body size using a 10‐year data set on black‐throated blue warblers (Setophaga caerulescens), a territorial species for which body size is hypothesized to mediate competition for mates. We found that direct selection on body size was weak and nonsignificant, as was social selection via the body size of the males' competitors. Analysing both types of selection simultaneously allows us to firmly reject a role for body size in competitive interactions between males and subsequent male fitness in this population. We evaluate the application of the sexual network approach to empirical data and suggest that other phenotypic traits such as song characteristics and plumage may be more relevant than body size for male–male competition in this small passerine bird.     

Sexual selection on male size drives the evolution of male‐biased sexual size dimorphism via the prolongation of male development

Sexual size dimorphism (SSD) arises when the net effects of natural and sexual selection on body size differ between the sexes. Quantitative SSD variation between taxa is common, but directional intraspecific SSD reversals are rare. We combined micro‐ and macroevolutionary approaches to study geographic SSD variation in closely related black scavenger flies. Common garden experiments revealed stark intra‐ and interspecific variation: Sepsis biflexuosa is monomorphic across the Holarctic, while S. cynipsea (only in Europe) consistently exhibits female‐biased SSD. Interestingly, S. neocynipsea displays contrasting SSD in Europe (females larger) and North America (males larger), a pattern opposite to the geographic reversal in SSD of S. punctum documented in a previous study. In accordance with the differential equilibrium model for the evolution of SSD, the intensity of sexual selection on male size varied between continents (weaker in Europe), whereas fecundity selection on female body size did not. Subsequent comparative analyses of 49 taxa documented at least six independent origins of male‐biased SSD in Sepsidae, which is likely caused by sexual selection on male size and mediated by bimaturism. Therefore, reversals in SSD and the associated changes in larval development might be much more common and rapid and less constrained than currently assumed.     

Patterns of sexual dimorphism in Mexican alligator lizards,Barisia imbricata

We compare morphological characteristics of male and female Barisia imbricata, Mexican alligator lizards, and find that mass, head length, coloration, incidence of scars from conspecifics, tail loss, and frequency of bearing the color/pattern of the opposite sex are all sexually dimorphic traits. Overall size (measured as snout–vent length), on the other hand, is not different between the two sexes. We use data on bite scar frequency and fecundity to evaluate competing hypotheses regarding the selective forces driving these patterns. We contend that sexual selection, acting through male‐male competition, may favor larger mass and head size in males, whereas large females are likely favored by natural selection for greater fecundity. In addition, the frequency of opposite‐sex patterning in males versus females may indicate that the costs of agonistic interactions among males are severe enough to allow for an alternative mating strategy. Finally, we discuss how sexual and natural selective forces may interact to drive or mask the evolution of sexually dimorphic traits.     

Natural and sexual selection on a plumage signal of status and on morphology in house sparrows,Passer domesticus

Temporal patterns of natural and sexual selection on male badge size and body traits were studied in a population of house sparrows, Passer domesticus. Badge size was a heritable trait as revealed by a significant father-son regression. Survival during autumn dispersal and winter was not related to badge size or body traits in yearling male house sparrows. Badges that signal dominance status were affected positively by directional selection for mating. Adult male house sparrows suffered an opposing selection pressure on badge size during autumn. Contrary to males, female house sparrows did not experience significant directional or stabilizing selection on any body trait. Directional sexual selection on male badge size due to female choice moves male sparrows away from their survival optimum. Opposing directional natural selection on badge size due to autumn mortality caused by predation maintains a stable badge size.     

SEXUAL SELECTION CAN REMOVE AN EXPERIMENTALLY INDUCED MUTATION LOAD

Sexual selection is argued to be important for the removal of deleterious mutations, promoting population fitness, accelerating adaptation, and compensating for the two‐fold cost of sex. Here we induced mutations in the dung beetle Onthophagus taurus using ionizing radiation, and tested the efficacy of sexual selection in their removal. Mutations reduced male precopulatory (strength) and postcopulatory (testes mass) sexual traits. Two generations of sexual selection were sufficient to remove mutations that affected male strength, but not testes mass. Induced mutations did not affect female productivity, which was elevated by sexual selection. Our results provide empirical support for the hypothesis that condition‐dependent traits offer a large target for mutational variation, and that sexual selection can purge the genome of deleterious mutations and promote population fitness.     

Male mating success in a North American pitviper: influence of body size,testosterone, and spatial metrics

Males with enhanced traits relative to conspecifics often show increased mating and reproductive success and thus have a fitness advantage. The opportunity or potential for sexual selection is predicted to occur under these conditions. Here, we investigated proximate determinants of mating success in male copperhead snakes (Agkistrodon contortrix), a medium‐sized pitviper of North America. Specifically, we investigated the relationships of body size (snout‐vent length, body mass), body condition index, spatial metrics (total distance moved, home range size), and plasma testosterone concentration on mating success in males. The single mating season lasts from August through September. We compared a set of candidate linear mixed models and selected the best‐fitting one using the adjusted Akaike Information Criterion (AICc). The AICc‐selected model (model 2), with testosterone, body condition index, and home range size as predictor variables, showed that male mating success was positively correlated with testosterone. To our knowledge, this is the first report to show the relationship of testosterone and individual mating success in any snake species. A parallel study conducted on male fitness in A. contortrix of the same population used microsatellite markers to assign parentage of fathers (known mothers). Unlike our study, they found that snout‐vent length was positively correlated with reproductive success and that males were experiencing greater sexual selection. This relationship has been detected under natural conditions in other species of snakes. Although behavioural data are important in any mating system analysis, they should not stand alone to infer parentage, relationships or selection metrics (e.g. Bateman gradients). Long‐term sperm storage by females, female cryptic choice, and other factors contribute to the complexity of mating success of males. Accordingly, we thus conclude that estimates of reproductive success and fitness in cryptic species, such as copperheads and other snakes, require robust molecular methods to draw accurate conclusions regarding proximate and evolutionary responses. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 185–194.     

A change in competitive context reverses sexual selection on male size

In studies of sexual selection, larger size is often argued to increase male fitness, and relatively smaller males are explained by genetic and/or environmental variation. We demonstrate that a size–development life‐history trade‐off could underlie the maintenance of a broad, unimodal distribution of size in male redback spiders (Latrodectus hasselti). Larger males are superior in direct competition, but redback males mature rapidly at small size in the presence of females. In field enclosures, we simulated two competitive contexts favouring development of divergent male sizes. Relatively smaller males lost when competing directly, but had 10 times higher fitness than relatively larger males when given the temporal advantage of rapid development. Linear selection gradients confirmed the reversal of selection on size, showing that it is critical to consider life‐history decisions underlying the development of traits related to fitness.     

Sexual selection and temporal phenotypic variation in a damselfly population

Temporal variation in selection can be generated by temporal variation in either the fitness surface or phenotypic distributions around a static fitness surface, or both concurrently. Here, we use within- and between-generation sampling of fitness surfaces and phenotypic distributions over 2 years to investigate the causes of temporal variation in the form of sexual selection on body size in the damselfly Enallagma aspersum. Within a year, when the average female body size differed substantially from the average male body size, male body size experienced directional selection. In contrast, when male and female size distributions overlapped, male body size experienced stabilizing selection when variances in body size were large, but no appreciable selection when the variances in body size were small. The causes of temporal variation in the form of selection can only be inferred by accounting for changes in both the fitness surface and changes in the distribution of phenotypes.     

Body size evolution in an old insect order: No evidence for Cope's Rule in spite of fitness benefits of large size

We integrate field data and phylogenetic comparative analyses to investigate causes of body size evolution and stasis in an old insect order: odonates (“dragonflies and damselflies”). Fossil evidence for “Cope's Rule” in odonates is weak or nonexistent since the last major extinction event 65 million years ago, yet selection studies show consistent positive selection for increased body size among adults. In particular, we find that large males in natural populations of the banded demoiselle (Calopteryx splendens) over several generations have consistent fitness benefits both in terms of survival and mating success. Additionally, there was no evidence for stabilizing or conflicting selection between fitness components within the adult life‐stage. This lack of stabilizing selection during the adult life‐stage was independently supported by a literature survey on different male and female fitness components from several odonate species. We did detect several significant body size shifts among extant taxa using comparative methods and a large new molecular phylogeny for odonates. We suggest that the lack of Cope's rule in odonates results from conflicting selection between fitness advantages of large adult size and costs of long larval development. We also discuss competing explanations for body size stasis in this insect group.     

Sexual selection on spontaneous mutations strengthens the between‐sex genetic correlation for fitness

A proposed benefit to sexual selection is that it promotes purging of deleterious mutations from populations. For this benefit to be realized, sexual selection, which is usually stronger on males, must purge mutations deleterious to both sexes. Here, we experimentally test the hypothesis that sexual selection on males purges deleterious mutations that affect both male and female fitness. We measured male and female fitness in two panels of spontaneous mutation‐accumulation lines of the fly, Drosophila serrata, each established from a common ancestor. One panel of mutation accumulation lines limited both natural and sexual selection (LS lines), whereas the other panel limited natural selection, but allowed sexual selection to operate (SS lines). Although mutation accumulation caused a significant reduction in male and female fitness in both the LS and SS lines, sexual selection had no detectable effect on the extent of the fitness reduction. Similarly, despite evidence of mutational variance for fitness in males and females of both treatments, sexual selection had no significant impact on the amount of mutational genetic variance for fitness. However, sexual selection did reshape the between‐sex correlation for fitness: significantly strengthening it in the SS lines. After 25 generations, the between‐sex correlation for fitness was positive but considerably less than one in the LS lines, suggesting that, although most mutations had sexually concordant fitness effects, sex‐limited, and/or sex‐biased mutations contributed substantially to the mutational variance. In the SS lines this correlation was strong and could not be distinguished from unity. Individual‐based simulations that mimick the experimental setup reveal two conditions that may drive our results: (1) a modest‐to‐large fraction of mutations have sex‐limited (or highly sex‐biased) fitness effects, and (2) the average fitness effect of sex‐limited mutations is larger than the average fitness effect of mutations that affect both sexes similarly.     

Measuring sexual selection on females in sex‐role‐reversed Mormon crickets (Anabrus simplex,Orthoptera: Tettigoniidae)

Although many studies examine the form of sexual selection in males, studies characterizing this selection in females remain sparse. Sexual selection on females is predicted for sex‐role‐reversed Mormon crickets, Anabrus simplex, where males are choosy of mates and nutrient‐deprived females compete for matings and nutritious nuptial gifts. We used selection analyses to describe the strength and form of sexual selection on female morphology. There was no positive linear sexual selection on the female body size traits predicted to be associated with male preferences and female competition. Instead, we detected selection for decreasing head width and mandible length, with stabilizing selection as the dominant form of nonlinear selection. Additionally, we tested the validity of a commonly used instantaneous measure of mating success by comparing selection results with those determined using cumulative mating rate. The two fitness measures yielded similar patterns of selection, supporting the common sampling method comparing mated and unmated fractions.     

Multivariate intralocus sexual conflict in seed beetles

Intralocus sexual conflict (IaSC) is pervasive because males and females experience differences in selection but share much of the same genome. Traits with integrated genetic architecture should be reservoirs of sexually antagonistic genetic variation for fitness, but explorations of multivariate IaSC are scarce. Previously, we showed that upward artificial selection on male life span decreased male fitness but increased female fitness compared with downward selection in the seed beetle Callosobruchus maculatus. Here, we use these selection lines to investigate sex‐specific evolution of four functionally integrated traits (metabolic rate, locomotor activity, body mass, and life span) that collectively define a sexually dimorphic life‐history syndrome in many species. Male‐limited selection for short life span led to correlated evolution in females toward a more male‐like multivariate phenotype. Conversely, males selected for long life span became more female‐like, implying that IaSC results from genetic integration of this suite of traits. However, while life span, metabolism, and body mass showed correlated evolution in the sexes, activity did not evolve in males but, surprisingly, did so in females. This led to sexual monomorphism in locomotor activity in short‐life lines associated with detrimental effects in females. Our results thus support the general tenet that widespread pleiotropy generates IaSC despite sex‐specific genetic architecture.     

Intralocus sexual conflict,adaptive sex allocation,and the heritability of fitness

Intralocus sexual conflict arises when selection favours alternative fitness optima in males and females. Unresolved conflict can create negative between‐sex genetic correlations for fitness, such that high‐fitness parents produce high‐fitness progeny of their same sex, but low‐fitness progeny of the opposite sex. This cost of sexual conflict could be mitigated if high‐fitness parents bias sex allocation to produce more offspring of their same sex. Previous studies of the brown anole lizard (Anolis sagrei) show that viability selection on body size is sexually antagonistic, favouring large males and smaller females. However, sexual conflict over body size may be partially mitigated by adaptive sex allocation: large males sire more sons than daughters, whereas small males sire more daughters than sons. We explored the evolutionary implications of these phenomena by assessing the additive genetic (co)variance of fitness within and between sexes in a wild population. We measured two components of fitness: viability of adults over the breeding season, and the number of their progeny that survived to sexual maturity, which includes components of parental reproductive success and offspring viability (RS^V). Viability of parents was not correlated with adult viability of their sons or daughters. RS^V was positively correlated between sires and their offspring, but not between dams and their offspring. Neither component of fitness was significantly heritable, and neither exhibited negative between‐sex genetic correlations that would indicate unresolved sexual conflict. Rather, our results are more consistent with predictions regarding adaptive sex allocation in that, as the number of sons produced by a sire increased, the adult viability of his male progeny increased.     

MALE‐SPECIFIC GENOTYPE BY ENVIRONMENT INTERACTIONS INFLUENCE VIABILITY SELECTION ACTING ON A SEXUALLY SELECTED INVERSION SYSTEM IN THE SEAWEED FLY,COELOPA FRIGIDA

In the seaweed fly, Coelopa frigida, a large chromosomal inversion system is affected by sexual selection and viability selection. However, our understanding of the interaction between these two selective forces is currently limited as research has focused upon a limited range of environments. We allowed C. frigida larvae to develop in two different algae, Fucus and Laminaria, and then measured viability and body size for each inversion genotype. Significant male‐specific genotype‐by‐environment interactions influenced viability and body size. For males developing in Laminaria, the direction of viability selection acts similarly on the inversion system as the direction of sexual selection. In contrast, for males developing in Fucus, viability selection opposes sexual selection. These results demonstrate that through considering viability selection in different environments, the costs and benefits associated with sexual selection can be found to vary.     

Population density mediates the interaction between pre‐ and postmating sexual selection

When females mate with more than one male, sexual selection acts both before and after mating. The interaction between pre‐ and postmating episodes of selection is expected to be context dependent, but few studies have investigated how total sexual selection changes under different ecological conditions. We examined how population density mediates the interaction between pre‐ and postmating sexual selection by establishing replicate populations of the horned dung beetle Onthophagus taurus at low, medium, and high densities, and then using microsatellite‐based parentage analyses to measure male fitness. We found that mating success and fertilization success were positively correlated at all three densities, but the strength of the correlation decreased with increasing density. We also found a shift from negative to positive linear selection on testes mass as density increased, and opposing selection on weapons and testes at high densities. These patterns suggest that the importance of postmating processes increases with increasing population density, which reduces the selective advantage of weapons for premating contest competition, and increases the selective advantage of large ejaculates for postmating sperm competition. We expect that density‐dependent selection on testes mass has contributed to the phenotypic variation observed between natural populations of O. taurus that differ in density.     

Quantifying selection on standard metabolic rate and body mass in Drosophila melanogaster

Standard metabolic rate (SMR), defined as the minimal energy expenditure required for self‐maintenance, is a key physiological trait. Few studies have estimated its relationship with fitness, most notably in insects. This is presumably due to the difficulty of measuring SMR in a large number of very small individuals. Using high‐throughput flow‐through respirometry and a Drosophila melanogaster laboratory population adapted to a life cycle that facilitates fitness measures, we quantified SMR, body mass, and fitness in 515 female and 522 male adults. We used a novel multivariate approach to estimate linear and nonlinear selection differentials and gradients from the variance‐covariance matrix of fitness, SMR, and body mass, allowing traits specific covariates to be accommodated within a single model. In males, linear selection differentials for mass and SMR were positive and individually significant. Selection gradients were also positive but, despite substantial sample sizes, were nonsignificant due to increased uncertainty given strong SMR‐mass collinearity. In females, only nonlinear selection was detected and it appeared to act primarily on body size, although the individual gradients were again nonsignificant. Selection did not differ significantly between sexes although differences in the fitness surfaces suggest sex‐specific selection as an important topic for further study.     

Intraspecific mating system evolution and its effect on complex male secondary sexual traits: Does male–male competition increase selection on size or shape?

Sexual selection is generally held responsible for the exceptional diversity in secondary sexual traits in animals. Mating system evolution is therefore expected to profoundly affect the covariation between secondary sexual traits and mating success. Whereas there is such evidence at the interspecific level, data within species remain scarce. We here investigate sexual selection acting on the exaggerated male fore femur and the male wing in the common and widespread dung flies Sepsis punctum and S. neocynipsea (Diptera: Sepsidae). Both species exhibit intraspecific differences in mating systems and variation in sexual size dimorphism (SSD) across continents that correlates with the extent of male–male competition. We predicted that populations subject to increased male–male competition will experience stronger directional selection on the sexually dimorphic male foreleg. Our results suggest that fore femur size, width and shape were indeed positively associated with mating success in populations with male‐biased SSD in both species, which was not evident in conspecific populations with female‐biased SSD. However, this was also the case for wing size and shape, a trait often assumed to be primarily under natural selection. After correcting for selection on overall body size by accounting for allometric scaling, we found little evidence for independent selection on any of these size or shape traits in legs or wings, irrespective of the mating system. Sexual dimorphism and (foreleg) trait exaggeration is therefore unlikely to be driven by direct precopulatory sexual selection, but more so by selection on overall size or possibly selection on allometric scaling.     

Nuptial gifts and the evolution of male body size

In many insect systems, males donate nuptial gifts to insure an effective copulation or as a form of paternal investment. However, if gift magnitude is both body size-limited and positively related to fitness, then the opportunity exists for the gift to promote the evolution of large male size. In the striped ground cricket, Allonemobius socius, males transfer a body size-limited, somatic nuptial gift that is comprised primarily of hemolymph. To address the implications of this gift on male size evolution, we quantified the intensity and direction of natural (fecundity) and sexual (mating success) selection over multiple generations. We found that male size was under strong positive sexual selection throughout the breeding season. This pattern of selection was similar in successive generations spanning multiple years. Male size was also under strong natural selection, with the largest males siring the most offspring. However, multivariate selection gradients indicated that gift size, and not male size, was the best predictor of female fecundity. In other words, direct fecundity selection for larger gifts placed indirect positive selection on male body size, supporting the hypothesis that nuptial gifts can influence the evolution of male body size in this system. Although female size was also under strong selection due to a size related fecundity advantage, it did not exceed selection on male size. The implications of these results with regard to the maintenance of the female-biased size dimorphic system are discussed.     

Autosomal variation for male body size and sperm competition phenotypes is uncorrelated in Drosophila melanogaster

Correlations between male body size and phenotypes impacting post-copulatory sexual selection are commonly observed during the manipulation of male body size by environmental rearing conditions. Here, we control for environmental influences and test for genetic correlations between natural variation in male body size and phenotypes affecting post-copulatory sexual selection in Drosophila melanogaster. Dry weights of virgin males from 90 second-chromosome and 88 third-chromosome substitution lines were measured. Highly significant line effects (p<0.001) documented a genetic basis to variation in male body size. No significant correlations were identified between male body size and the components of sperm competitive ability. These results suggest that natural autosomal variation for male body size has little impact on post-copulatory sexual selection. If genetic correlations exist between male body size and post-copulatory sexual selection then variation in the sex chromosomes are likely candidates, as might be expected if sexually antagonistic coevolution was responsible.