Condition dependence and the maintenance of genetic variance in a sexually dimorphic black scavenger fly

The maintenance of genetic variation in traits under strong sexual selection is a longstanding problem in evolutionary biology. The genic capture model proposes that this problem can be explained by the evolution of condition dependence in exaggerated male traits. We tested the predictions that condition dependence should be more pronounced in male sexual traits and that genetic variance in expression of these traits should increase under stress as among‐genotype variation in overall condition is exposed. Genetic variance in female and nonsexual traits should, by contrast, be similar across environments as a result of stabilizing selection on trait expression. The relationship between the degree of sexual dimorphism, condition dependence and additive genetic variance (V_a) was assessed for two morphological traits (body size and relative fore femur width) affecting male mating success in the black scavenger fly Sepsis punctum (Diptera: Sepsidae) and for development time (a nonsexual trait often correlated with body size). We compared trait expression between the sexes for two cross‐continental populations that differ in degree of sexual dimorphism (Ottawa and Zurich). Condition dependence was indeed most pronounced in males of the strongly dimorphic Zurich population (males larger), and V_a was similar for males and females unless the trait was strongly sex specific and condition dependent. Contrary to prediction, however, V_a primarily increased under food limitation in both sexes, and genetic variance in fore femur width was low to nil, perhaps depleted by putatively strong sexual selection. Solely for body size of Zurich males, V_a increased more in males than females at limited food, in accordance with the predictions of the genic capture model. Overall therefore, quantitative genetic evidence in support of the model was inconsistent and weak at best.     

Spatiotemporal variation in selection on body size in the dung fly Sepsis cynipsea

Standardized measures of the strength of selection on a character allow quantitative comparisons across populations in time and space. Spatiotemporal variation in selection influences patterns of adaptation and the evolution of characters and must therefore be documented. For the dung-breeding fly Sepsis cynipsea, we document patterns of variation in sexual, fecundity and larval and adult viability selection on body size at several spatiotemporal scales: between-populations, over the season, over the day and between dung pats. Adult viability selection based on residual physiological survivorship in the laboratory was nil or weakly negative. In contrast, larval viability selection in two laboratory environments was weakly positive for males at low competition and females at high competition. Fecundity selection was positive and strong at all times and in all populations. Sexual selection reflecting pairing success was overall strongly positive (about three times stronger than fecundity selection), while selection reflecting male reproductive success via the clutch size of his mate (i.e. assortative mating) was essentially nil. Only sexual selection varied significantly at coarse (between populations and seasonally) but not at fine (within a day or between pats on a pasture) spatial and temporal scales. Quadratic and correlational selection differentials were low and inconsistent in all episodes except for fecundity selection, where there was some evidence that clutch size reaches an asymptote at large body sizes, implying weaker selection for large size as females get bigger. Implications of these results for the evolution of body size and body size dimorphism are discussed.     

Viability selection on female fly finery in the wild

Female ornaments have evolved in a few taxa in which females compete for access to important resources provided by their mates. However, the effects of these sexually selected traits on survival have not been studied. Elaborate leg‐scale and/or abdominal ornaments are displayed by females of some Rhamphomyia dance flies (Diptera: Empididae) to flying males carrying prey gifts (females do not hunt). Previous analyses have shown significant sexual selection on these female traits. We studied viability selection on the traits by sampling the webs of two spider species and comparing prey R. longicauda females to survivors. We also investigated viability selection from one of the spiders over two seasons. We found that the direction of viability selection on R. longicauda from sticky Tetragnatha spider webs was consistent over two seasons. For abdominal ornaments the form of viability selection was positive and primarily directional (linear). Viability selection also favoured shorter tibiae but there was no significant selection on the size of residual tibial scale area. However, with the addition of dance fly kills from the non‐sticky, leaf‐covering webs of a Dictyna spider, abundant in only one of the seasons, the overall direction of viability selection favoured larger tibial ornaments. While noting that this viability selection on tibial scale ornaments may be a statistical artefact of the fewer traits in the two‐predator analysis (abdominal structures were missing from most Dictyna prey), we suggest that simple differences in the natural history of selective agents causing mortality may partly explain the variation in whether sexual traits are under viability selection. Viability selection on ornamental traits may vary greatly between seasons with changes in the abundances of different natural enemies so that net directional selection on these traits over many generations may be weak.     

Inversion frequencies and phenotypic effects are modulated by the environment: insights from a reciprocal transplant study in <Emphasis Type="Italic">Coelopa frigida</Emphasis>

Understanding how environmental variation drives phenotypic diversification within species is a major objective in evolutionary biology. The seaweed fly Coelopa frigida provides an excellent model for the study of genetically driven phenotypes because it carries an α/β inversion polymorphism that affects body size. Coelopa frigida inhabits highly variable beds of decomposing seaweed on the coast in Scandinavia thus providing a suitable test ground to investigate the genetic effects of substrate on both the frequency of the inversion (directional selection) and on the phenotype (genotype?×?environment effects). Here we use a reciprocal transplant experiment to test the effect of the α/β inversion on body size traits and development time across four suitable natural breeding substrates from the clinal distribution. We show that while development time is unaffected by G?×?E effects, both the frequency of the inversion and the relative phenotypic effects of the inversion on body size differ between population?×?substrate combinations. This indicates that the environment modulates the fitness as well as the phenotypic effects of the inversion karyotypes. It further suggests that the inversion may have accumulated qualitatively different mutations in different populations that interact with the environment. Together our results are consistent with the idea that the inversion in C. frigida likely evolves via a combination of local mutation, G?×?E effects, and differential fitness of inversion karyotypes in heterogeneous environments.     

A novel method of comparing mating success and survival reveals similar sexual and viability selection for mobility traits in female tree crickets

The relationship between sexual and viability selection in females is necessarily different than that in males, as investment in sexual traits potentially comes at the expense of both fecundity and survival. Accordingly, females do not usually invest in sexually selected traits. However, direct benefits obtained from mating, such as nuptial gifts, may encourage competition among females and subsidize investment into sexually selected traits. We compared sexual and viability selection on female tree crickets Oecanthus nigricornis, a species where females mate frequently to obtain nuptial gifts and sexual selection on females is likely. If male choice determines female mating success in this species, we expect sexual selection for fecundity traits, as males of many species prefer more fecund females. Alternatively, intrasexual scramble or combat competition on females may select for larger jumping legs or wider heads (respectively). We estimated mating success in wild caught crickets using microsatellite analysis of stored sperm and estimated relative viability by comparing surviving female O. nigricornis to those captured by a common wasp predator. In support of the scramble competition hypothesis, we found sexual selection for females with larger hind legs and narrower heads. We also found stabilizing viability selection for intermediate head width and hind leg size. As predicted, traits under viability and sexual selection were very similar, and the direction of that selection was not opposing. However, because the shape of sexual and viability selection differs, these episodes of selection may favour slightly different trait sizes.     

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.     

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.     

Allometry of a sexual trait in relation to diet experience and alternative mating tactics in two rubyspot damselflies (Calopterygidae: Hetaerina)

Several arguments have been put forward to explain how sexual selection drives the evolution of sexual trait allometry, especially hyperallometry. The ‘positive allometry theory’ suggests that hyperallometry is a rule in all‐secondary sexual traits, whereas the ‘display hypothesis’ suggests that only males in good condition will exhibit hyperallometric sexual display traits. In the present study, we investigated: (1) the condition‐dependence nature (by using two diet treatments that varied in the amount of food provided to the larvae) of a sexually selected trait (wing pigmentation; WP) in recently‐emerged adults of the American rubyspot damselfly, Hetaerina americana, and (2) the scaling relationship between WP and body size (wing and body length) in the rubyspot damselflies H. americana and Hetaerina vulnerata, according to alternative reproductive tactics (ARTs; territorial and nonterritorial males). First, we found support that indicated that diet positively affected WP length, although there was no significant WP allometric pattern in relation to diet regimes. Second, WP was hyperallometric in both Hetaerina species. WP size was similar between ARTs and, in H. americana (but not H. vulnerata), nonterritorial males showed steeper slopes than territorial males when wing length was used. The results obtained support the notion that sexual traits are hyperallometric, although there is no clear pattern in relation to ARTs. © 2013 The Linnean Society of London     

Genome‐wide selection components analysis in a fish with male pregnancy

A major goal of evolutionary biology is to identify the genome‐level targets of natural and sexual selection. With the advent of next‐generation sequencing, whole‐genome selection components analysis provides a promising avenue in the search for loci affected by selection in nature. Here, we implement a genome‐wide selection components analysis in the sex role reversed Gulf pipefish, Syngnathus scovelli. Our approach involves a double‐digest restriction‐site associated DNA sequencing (ddRAD‐seq) technique, applied to adult females, nonpregnant males, pregnant males, and their offspring. An F_ST comparison of allele frequencies among these groups reveals 47 genomic regions putatively experiencing sexual selection, as well as 468 regions showing a signature of differential viability selection between males and females. A complementary likelihood ratio test identifies similar patterns in the data as the F_ST analysis. Sexual selection and viability selection both tend to favor the rare alleles in the population. Ultimately, we conclude that genome‐wide selection components analysis can be a useful tool to complement other approaches in the effort to pinpoint genome‐level targets of selection in the wild.     

GENETIC CORRELATION BETWEEN A FEMALE MATING PREFERENCE AND THE PREFERRED MALE CHARACTER IN SEAWEED FLIES (COELOPA FRIGIDA)

The mating preferences of female seaweed flies Coelopa frigida were determined by observing their acceptance or rejection of males of known size. The inversion karyotype of both males and females was also determined. Females exhibited a preference to mate with large males, and evidence is presented that a genetic correlation exists between the female preference and the preferred trait. Females carrying the inversion karyotype associated with large male size showed a strong preference for large males; females carrying the inversion associated with small male size also exhibited a preference for large males, but it was significantly less strong. This finding suggests that a Fisherian process may be operating.     

Sexual dimorphism of head morphology in three‐spined stickleback Gasterosteus aculeatus

This study examined sexual dimorphism of head morphology in the ecologically diverse three‐spined stickleback Gasterosteus aculeatus. Male G. aculeatus had longer heads than female G. aculeatus in all 10 anadromous, stream and lake populations examined, and head length growth rates were significantly higher in males in half of the populations sampled, indicating that differences in head size increased with body size in many populations. Despite consistently larger heads in males, there was significant variation in size‐adjusted head length among populations, suggesting that the relationship between head length and body length was flexible. Inter‐population differences in head length were correlated between sexes, thus population‐level factors influenced head length in both sexes despite the sexual dimorphism present. Head shape variation between lake and anadromous populations was greater than that between sexes. The common divergence in head shape between sexes across populations was about twice as important as the sexual dimorphism unique to each population. Finally, much of the sexual dimorphism in head length was due to divergence in the anterior region of the head, where the primary trophic structures were found. It is unclear whether the sexual dimorphism was due to natural selection for niche divergence between sexes or sexual selection. This study improves knowledge of the magnitude, growth rate divergence, inter‐population variation and location of sexual dimorphism in G. aculeatus head morphology.     

Positive genetic correlation between brain size and sexual traits in male guppies artificially selected for brain size

Brain size is an energetically costly trait to develop and maintain. Investments into other costly aspects of an organism's biology may therefore place important constraints on brain size evolution. Sexual traits are often costly and could therefore be traded off against neural investment. However, brain size may itself be under sexual selection through mate choice on cognitive ability. Here, we use guppy (Poecilia reticulata) lines selected for large and small brain size relative to body size to investigate the relationship between brain size, a large suite of male primary and secondary sexual traits, and body condition index. We found no evidence for trade‐offs between brain size and sexual traits. Instead, larger‐brained males had higher expression of several primary and precopulatory sexual traits – they had longer genitalia, were more colourful and developed longer tails than smaller‐brained males. Larger‐brained males were also in better body condition when housed in single‐sex groups. There was no difference in post‐copulatory sexual traits between males from the large‐ and small‐brained lines. Our data do not support the hypothesis that investment into sexual traits is an important limiting factor to brain size evolution, but instead suggest that brain size and several sexual traits are positively genetically correlated.     

Sexual selection constrains the body mass of male but not female mice

Sexual size dimorphism results when female and male body size is influenced differently by natural and sexual selection. Typically, in polygynous species larger male body size is thought to be favored in competition for mates and constraints on maximal body size are due to countervailing natural selection on either sex; however, it has been postulated that sexual selection itself may result in stabilizing selection at an optimal mass. Here we test this hypothesis by retrospectively assessing the influence of body mass, one metric of body size, on the fitness of 113 wild‐derived house mice (Mus musculus) residing within ten replicate semi‐natural enclosures from previous studies conducted by our laboratory. Enclosures possess similar levels of sexual selection, but relaxed natural selection, relative to natural systems. Heavier females produced more offspring, while males of intermediate mass had the highest fitness. Female results suggest that some aspect of natural selection, absent from enclosures, acts to decrease their body mass, while the upper and lower boundaries of male mass are constrained by sexual selection.     

Sexual selection versus alternative causes of sexual dimorphism in teiid lizards

Summary The presence and extent of sexual dimorphisms in body form (size and shape) of adult macroteiid lizards were investigated. Males were significantly larger than females in the temperate species, Cnemidophorus tigris, and in the tropical species, Ameiva ameiva and C. ocellifer. Young adult C. tigris males grew faster than young adult females within and between reproductive seasons. Adult males of all species had larger heads than adult females of the same body size; this difference increased with body size. Moreover, male C. tigris were heavier than females of the same snout-vent length. The causes and consequences of the sexual dimorphisms were also examined. The possible causes of body size are especially numerous, and distinguishing the relative influences of the various causal selection factors on body size is problematical. Nevertheless, observational field data were used to tentatively conclude that intrasexual selection was the cause of larger body size of C. tigris males relative to females because (1) larger males won in male aggressive interactions, (2) the winning males gained access to more females by repelling competitors and by female acceptance, (3) larger males consequently had higher reproductive success, and (4) other hypothetical causes of larger male size were unsupported.     

On the role of sexual selection in ecological divergence: a test of body‐size assortative mating in the eastern newt Notophthalmus viridescens

Speciation processes initiated by divergent selection often fail to complete; yet, how sexual selection is involved in the progress of ecological speciation is rarely understood. Intraspecific body‐size variation affects mate preference and male–male competition, which can consequently lead to assortative mating based on body size. In the present study, we tested the importance of body size difference in the potential of assortative mating between the two eastern newt subspecies, larger Notophthalmus viridescens viridescens and smaller Notophthalmus viridescens dorsalis. Through differential expression of life‐cycle polyphenism, these two subspecies are adapted to contrasting environments, which has likely led to the subspecific body‐size difference. We found that males of both subspecies preferred larger females of N. v. viridescens as mates presumably because of the fecundity advantage of larger females. On the other hand, no evidence of female choice was found. Larger males of N. v. viridescens exhibited greater competitive ability and gained primary access to larger females of their own kind. However, smaller males were able to overcome their inferior competitive ability by interfering with larger males' spermatophore transfer and sneakily mating with larger females. Thus, the subspecific body‐size difference importantly affected sexual selection processes, resulting in nonrandom but not completely assortative mating patterns between the larger and smaller subspecies. Although life‐cycle polyphenism facilitates the intraspecific ecological divergence within N. v. viridescens sexual selection processes, namely smaller males' mate preference for larger females and sexual interference during spermatophore transfer, may be halting completion of the ecological speciation. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 884–897.     

Scaling of Size and Dimorphism in Primates I: Microevolution

I used a new quantitative genetics model to predict relationships between sex-specific body size and sex-specific relative variability when populations experience differences in relative intensity of sex-specific selection pressures—stronger selection on males or females—and direction of selection: increase or decrease in size. I combined Lande's (Evolution 34: 292–305) model for the response of sex-specific means to selection with a newly derived generalization of Bulmer's (Am. Nat. 105: 201–211) model for the response of relative variability to selection. I used this combined response model to predict correlations of sex-specific size and relative variability under various starting conditions, which one can compare to correlations between closely related primate populations. One can then compare predicted patterns of sex-specific selection pressures to social and ecological variables pertaining to those populations to identify likely forces producing microevolutionary change in sexual size dimorphism (SSD). I provide examples of this approach for populations representing three taxa: Papio anubis, Saguinus mystax, and Cercopithecus aethiops pygerythrus. Model results suggest that microevolutionary changes in SSD can result from greater selection acting on males or females, and that natural selection or natural and sexual selection combined, rather than sexual selection alone, may sometimes explain sex-specific selection differentials.     

Growth and survivorship as proximate causes of sexual size dimorphism in peninsula dragon lizards Ctenophorus fionni

Males and females differ in body size in many animals, but the direction and extent of this sexual size dimorphism (SSD) varies widely. Males are larger than females in most lizards of the iguanian clade, which includes dragon lizards (Agamidae). I tested whether the male larger pattern of SSD in the peninsula dragon lizard, Ctenophorus fionni, is a result of sexual selection for large male size or relatively higher mortality among females. Data on growth and survivorship were collected from wild lizards during 1991–1994. The likelihood of differential predation between males and females was assessed by exposing pairs of male and female lizards to a predator in captivity, and by comparing the frequency of tail damage in wild‐caught males and females. Male and female C. fionni grew at the same rate, but males grew for longer than females and reached a larger asymptotic size (87 mm vs. 78 mm). Large males were under‐represented in the population because they suffered higher mortality than females. Predation may account for some of this male‐biased mortality. The male‐biased SSD in C. fionni resulted from differences in growth pattern between the sexes. The male‐biased SSD was not the result of proximate factors reducing female body size. Indeed SSD in this species remained male‐biased despite high mortality among large males. SSD in C. fionni is consistent with the ultimate explanation of sexual selection for large body size in males.     

Do male secondary sexual characters signal ejaculate quality? A meta‐analysis

There are two reasons why researchers are interested in the phenotypic relationship between the expression of male secondary sexual characters (SSCs) and ‘ejaculate quality’ (defined as sperm/ejaculate traits that are widely assumed to increase female fertility and/or sperm competitiveness). First, if the relationship is positive then females could gain a direct benefit by choosing more attractive males for fertility assurance reasons (‘the phenotype‐linked fertility’ hypothesis). Second, there is much interest in the direction of the correlation between traits favoured by pre‐copulatory sexual selection (i.e. affecting mating success) and those favoured by post‐copulatory sexual selection (i.e. increasing sperm competitiveness). If the relationship is negative this could lead to the two forms of selection counteracting each other. Theory predicts that the direction of the relationship could be either positive or negative depending on the underlying genetic variance and covariance in each trait, the extent of variation among males in condition (resources available to allocate to reproductive traits), and variation among males in the cost or rate of mating. We conducted a meta‐analysis to determine the average relationship between the expression of behavioural and morphological male secondary sexual characters and four assays of ejaculate quality (sperm number, viability, swimming speed and size). Regardless of how the data were partitioned the mean relationship was consistently positive, but always statistically non‐significant. The only exception was that secondary sexual character expression was weakly but significantly positively correlated with sperm viability (r = 0.07, P < 0.05). There was no significant difference in the strength or direction of the relationship between behavioural and morphological SSCs, nor among relationships using the four ejaculate quality assays. The implications of our findings are discussed.     

Stronger condition dependence in female size explains altitudinal variation in sexual size dimorphism of a Tibetan frog

The present study investigated altitudinal variation in sexual size dimorphism of a Tibetan frog Nanorana parkeri. Size dimorphism was female‐biased in all populations, although this bias became less at higher altitudes because of a steeper altitudinal decrease in female size than male size. Operational sex ratios, an indicator of the opportunity for sexual selection on larger males, changed independently of altitude. Clutch volume, an indicator of the strength of fecundity selection on larger females, was positively with female size, and tended to decrease approaching high altitudes. Females lived longer and grew more slowly than males, and the mean age in both sexes increased and growth rate decreased altitudinally, although the changes were more rapid in females than males. These results suggest that, relative to males, females (i.e. the sex that typically bears greater reproductive costs and experiences stronger directional selection for larger size to take fecundity advantages) should be more sensitive to environments, attaining a larger size via enhancing growth under favourable lower‐latitude conditions but a smaller size as a result of retarding growth when conditions become harsher at higher altitudes. This supports the condition‐dependence hypothesis with respect to intraspecific variation in sexual size dimorphism. © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 558–565.     

Distribution and composition of colony founding associations of a subterranean termite, Reticulitermes kanmonensis

We investigated distribution and sexual composition of founding associations of Reticulitermes kanmonensis, the Japanese subterranean termite, which occurs only in the Kanmon area. These properties are discussed in relation to body size and mitochondrial genotype of the dealates. The founding colonies showed a highly aggregated distribution with a ‘hot spot’ of colony founding; however, mitochondrial haplotypes of the dealates suggested random mating. Monogamous colonies were predominant, but solitary colonies and colonies with two females and/or males also occurred. Paired dealates tended to be larger than solitary founders, suggesting that both sexes were under sexual selection related to body size.