Conservation of multivariate female preference functions and preference mechanisms in three species of trilling field crickets

Divergence in mate recognition systems among closely related species is an important contributor to assortative mating and reproductive isolation. Here, we examine divergence in male song traits and female preference functions in three cricket species with songs consisting of long trills. The shape of female preference functions appears to be mostly conserved across species and follows the predictions from a recent model for song recognition. Multivariate preference profiles, combining the pulse and trill parameters, demonstrate selectivity for conspecific pulse rates and high trill duty cycles. The rules for integration across pulse and trill timescales were identical for all three species. Generally, we find greater divergence in male song traits than in associated female preferences. For pulse rate, we find a strong match between divergent male traits and female peak preferences. Preference functions for trill parameters and carrier frequency are similar between species and show less congruence between signal and preference. Differences among traits in the degree of trait–preference (mis)match may reflect the strength of preferences and the potential for linkage disequilibrium, selective constraints and alternative selective pressures, but appear unrelated to selection for mate recognition per se.     

Temporal variation in selection on male and female traits in wild tree crickets

Understanding temporal variation in selection in natural populations is necessary to accurately estimate rates of divergence and macroevolutionary processes. Temporal variation in the strength and direction of selection on sex‐specific traits can also explain stasis in male and female phenotype and sexual dimorphism. I investigated changes in strength and form of viability selection (via predation by wasps) in a natural population of male and female tree crickets over 4 years. I found that although the source of viability stayed the same, viability selection affected males and females differently, and the strength, direction and form of selection varied considerably from year to year. In general, males experienced significant linear selection and significant selection differentials more frequently than females, and different male traits experienced significant linear selection each year. This yearly variation resulted in overall weak but significant convex selection on a composite male trait that mostly represented leg size and wing width. Significant selection on female phenotype was uncommon, but when it was detected, it was invariably nonlinear. Significant concave selection on traits representing female body size was observed in some years, as the largest and smallest females were preyed on less (the largest may have been too heavy for flying wasps to carry). Viability selection was significantly different between males and females in 2 of 4 years. Although viability selection via predation has the potential to drive phenotypic change and sexual dimorphism, temporal variation in selection may maintain stasis.     

Species divergence in field crickets: genetics,song, ecomorphology,and pre‐ and postzygotic isolation

Studies that simultaneously estimate levels of species divergence in genetics, reproductive and ecological traits, and pre‐ and postzygotic isolation are relatively rare. Here we compare levels of divergence in three allopatric sister species of field crickets. We compare divergence in both nuclear and mitochondrial DNA, male song, female ovipositor length, levels of pre‐ and postzygotic isolation, and male versus female contributions to prezygotic isolation. Taken together, our data show the accumulation of a multitude of potential reproductive isolating barriers if secondary contact were to become established. Furthermore, ecological and behavioural prezygotic isolation appear significantly more advanced than postzygotic isolation, with prezygotic isolation due to female behaviour exceeding that due to male behaviour.     

Female choice for male cuticular hydrocarbon profile in decorated crickets is not based on similarity to their own profile

Indirect genetic benefits derived from female mate choice comprise additive (good genes) and nonadditive genetic benefits (genetic compatibility). Although good genes can be revealed by condition‐dependent display traits, the mechanism by which compatibility alleles are detected is unclear because evaluation of the genetic similarity of a prospective mate requires the female to assess the genotype of the male and compare it to her own. Cuticular hydrocarbons (CHCs), lipids coating the exoskeleton of most insects, influence female mate choice in a number of species and offer a way for females to assess genetic similarity of prospective mates. Here, we determine whether female mate choice in decorated crickets is based on male CHCs and whether it is influenced by females' own CHC profiles. We used multivariate selection analysis to estimate the strength and form of selection acting on male CHCs through female mate choice, and employed different measures of multivariate dissimilarity to determine whether a female's preference for male CHCs is based on similarity to her own CHC profile. Female mating preferences were significantly influenced by CHC profiles of males. Male CHC attractiveness was not, however, contingent on the CHC profile of the choosing female, as certain male CHC phenotypes were equally attractive to most females, evidenced by significant linear and stabilizing selection gradients. These results suggest that additive genetic benefits, rather than nonadditive genetic benefits, accrue to female mate choice, in support of earlier work showing that CHC expression of males, but not females, is condition dependent.     

The mutation matrix and the evolution of evolvability

Evolvability is a key characteristic of any evolving system, and the concept of evolvability serves as a unifying theme in a wide range of disciplines related to evolutionary theory. The field of quantitative genetics provides a framework for the exploration of evolvability with the promise to produce insights of global importance. With respect to the quantitative genetics of biological systems, the parameters most relevant to evolvability are the G-matrix, which describes the standing additive genetic variances and covariances for a suite of traits, and the M-matrix, which describes the effects of new mutations on genetic variances and covariances. A population's immediate response to selection is governed by the G-matrix. However, evolvability is also concerned with the ability of mutational processes to produce adaptive variants, and consequently the M-matrix is a crucial quantitative genetic parameter. Here, we explore the evolution of evolvability by using analytical theory and simulation-based models to examine the evolution of the mutational correlation, r(mu), the key parameter determining the nature of genetic constraints imposed by M. The model uses a diploid, sexually reproducing population of finite size experiencing stabilizing selection on a two-trait phenotype. We assume that the mutational correlation is a third quantitative trait determined by multiple additive loci. An individual's value of the mutational correlation trait determines the correlation between pleiotropic effects of new alleles when they arise in that individual. Our results show that the mutational correlation, despite the fact that it is not involved directly in the specification of an individual's fitness, does evolve in response to selection on the bivariate phenotype. The mutational variance exhibits a weak tendency to evolve to produce alignment of the M-matrix with the adaptive landscape, but is prone to erratic fluctuations as a consequence of genetic drift. The interpretation of this result is that the evolvability of the population is capable of a response to selection, and whether this response results in an increase or decrease in evolvability depends on the way in which the bivariate phenotypic optimum is expected to move. Interestingly, both analytical and simulation results show that the mutational correlation experiences disruptive selection, with local fitness maxima at -1 and +1. Genetic drift counteracts the tendency for the mutational correlation to persist at these extreme values, however. Our results also show that an evolving M-matrix tends to increase stability of the G-matrix under most circumstances. Previous studies of G-matrix stability, which assume nonevolving M-matrices, consequently may overestimate the level of instability of G relative to what might be expected in natural systems. Overall, our results indicate that evolvability can evolve in natural systems in a way that tends to result in alignment of the G-matrix, the M-matrix, and the adaptive landscape, and that such evolution tends to stabilize the G-matrix over evolutionary time.     

Structure and stability of genetic variance–covariance matrices: A Bayesian sparse factor analysis of transcriptional variation in the three‐spined stickleback

The genetic variance–covariance matrix ( G ) is a quantity of central importance in evolutionary biology due to its influence on the rate and direction of multivariate evolution. However, the predictive power of empirically estimated G ‐matrices is limited for two reasons. First, phenotypes are high‐dimensional, whereas traditional statistical methods are tuned to estimate and analyse low‐dimensional matrices. Second, the stability of G to environmental effects and over time remains poorly understood. Using Bayesian sparse factor analysis (BSFG) designed to estimate high‐dimensional G ‐matrices, we analysed levels variation and covariation in 10,527 expressed genes in a large (n = 563) half‐sib breeding design of three‐spined sticklebacks subject to two temperature treatments. We found significant differences in the structure of G between the treatments: heritabilities and evolvabilities were higher in the warm than in the low‐temperature treatment, suggesting more and faster opportunity to evolve in warm (stressful) conditions. Furthermore, comparison of G and its phenotypic equivalent P revealed the latter is a poor substitute of the former. Most strikingly, the results suggest that the expected impact of G on evolvability—as well as the similarity among G ‐matrices—may depend strongly on the number of traits included into analyses. In our results, the inclusion of only few traits in the analyses leads to underestimation in the differences between the G ‐matrices and their predicted impacts on evolution. While the results highlight the challenges involved in estimating G , they also illustrate that by enabling the estimation of large G ‐matrices, the BSFG method can improve predicted evolutionary responses to selection.     

The probability of parallel genetic evolution from standing genetic variation

Parallel evolution is often assumed to result from repeated adaptation to novel, yet ecologically similar, environments. Here, we develop and analyse a mathematical model that predicts the probability of parallel genetic evolution from standing genetic variation as a function of the strength of phenotypic selection and constraints imposed by genetic architecture. Our results show that the probability of parallel genetic evolution increases with the strength of natural selection and effective population size and is particularly likely to occur for genes with large phenotypic effects. Building on these results, we develop a Bayesian framework for estimating the strength of parallel phenotypic selection from genetic data. Using extensive individual‐based simulations, we show that our estimator is robust across a wide range of genetic and evolutionary scenarios and provides a useful tool for rigorously testing the hypothesis that parallel genetic evolution is the result of adaptive evolution. An important result that emerges from our analyses is that existing studies of parallel genetic evolution frequently rely on data that is insufficient for distinguishing between adaptive evolution and neutral evolution driven by random genetic drift. Overcoming this challenge will require sampling more populations and the inclusion of larger numbers of loci.     

The complex interplay between macronutrient intake,cuticular hydrocarbon expression and mating success in male decorated crickets

The condition dependence of male sexual traits plays a central role in sexual selection theory. Relatively little, however, is known about the condition dependence of chemical signals used in mate choice and their subsequent effects on male mating success. Furthermore, few studies have isolated the specific nutrients responsible for condition‐dependent variation in male sexual traits. Here, we used nutritional geometry to determine the effect of protein (P) and carbohydrate (C) intake on male cuticular hydrocarbon (CHC) expression and mating success in male decorated crickets (Gryllodes sigillatus). We show that both traits are maximized at a moderate‐to‐high intake of nutrients in a P:C ratio of 1 : 1.5. We also show that female precopulatory mate choice exerts a complex pattern of linear and quadratic sexual selection on this condition‐dependent variation in male CHC expression. Structural equation modelling revealed that although the effect of nutrient intake on mating success is mediated through condition‐dependent CHC expression, it is not exclusively so, suggesting that other traits must also play an important role. Collectively, our results suggest that the complex interplay between nutrient intake, CHC expression and mating success plays an important role in the operation of sexual selection in G. sigillatus.     

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.     

Moderate heritability and low evolvability of sperm morphology in a species with high risk of sperm competition,the collared flycatcher Ficedula albicollis

Spermatozoa represent the morphologically most diverse type of animal cells and show remarkable variation in size across and also within species. To understand the evolution of this diversity, it is important to reveal to what degree this variation is genetic or environmental in origin and whether this depends on species’ life histories. Here we applied quantitative genetic methods to a pedigreed multigenerational data set of the collared flycatcher Ficedula albicollis, a passerine bird with high levels of extra‐pair paternity, to partition genetic and environmental sources of phenotypic variation in sperm dimensions for the first time in a natural population. Narrow‐sense heritability (h²) of total sperm length amounted to 0.44 ± 0.14 SE, whereas the corresponding figure for evolvability (estimated as coefficient of additive genetic variation, CV_a) was 0.02 ± 0.003 SE. We also found an increase in total sperm length within individual males between the arrival and nestling period. This seasonal variation may reflect constraints in the production of fully elongated spermatozoa shortly after arrival at the breeding grounds. There was no evidence of an effect of male age on sperm dimensions. In many previous studies on laboratory populations of several insect, mammal and avian species, heritabilities of sperm morphology were higher, whereas evolvabilities were similar. Explanations for the differences in heritability may include variation in the environment (laboratory vs. wild), intensity of sexual selection via sperm competition (high vs. low) and genetic architecture that involves unusual linkage disequilibrium coupled with overdominance in one of the studied species.     

The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

Sex‐linked inheritance,genetic correlations and sexual dimorphism in three melanin‐based colour traits in the barn owl

Theory states that genes on the sex chromosomes have stronger effects on sexual dimorphism than genes on the autosomes. Although empirical data are not necessarily consistent with this theory, this situation may prevail because the relative role of sex‐linked and autosomally inherited genes on sexual dimorphism has rarely been evaluated. We estimated the quantitative genetics of three sexually dimorphic melanin‐based traits in the barn owl (Tyto alba), in which females are on average darker reddish pheomelanic and display more and larger black eumelanic feather spots than males. The plumage traits with higher sex‐linked inheritance showed lower heritability and genetic correlations, but contrary to prediction, these traits showed less pronounced sexual dimorphism. Strong offspring sexual dimorphism primarily resulted from daughters not expressing malelike melanin‐based traits and from sons expressing femalelike traits to similar degrees as their sisters. We conclude that in the barn owl, polymorphism at autosomal genes rather than at sex‐linked genes generate variation in sexual dimorphism in melanin‐based traits.     

Polymorphisms in a desaturase 2 ortholog associate with cuticular hydrocarbon and male mating success variation in a natural population of Drosophila serrata

Elucidating the nature of genetic variation underlying both sexually selected traits and the fitness components of sexual selection is essential to understanding the broader consequences of sexual selection as an evolutionary process. To date, there have been relatively few attempts to connect the genetic variance in sexually selected traits with segregating DNA sequence polymorphisms. We set out to address this in a well‐characterized sexual selection system – the cuticular hydrocarbons (CHCs) of Drosophila serrata – using an indirect association study design that allowed simultaneous estimation of the genetic variance in CHCs, sexual fitness and single nucleotide polymorphism (SNP) effects in an outbred population. We cloned and sequenced an ortholog of the D. melanogaster desaturase 2 gene, previously shown to affect CHC biosynthesis in D. melanogaster, and associated 36 SNPs with minor allele frequencies > 0.02 with variance in CHCs and sexual fitness. Three SNPs had significant multivariate associations with CHC phenotype (q‐value < 0.05). At these loci, minor alleles had multivariate effects on CHCs that were weakly associated with the multivariate direction of sexual selection operating on these traits. Two of these SNPs had pleiotropic associations with male mating success, suggesting these variants may underlie responses to sexual selection due to this locus. There were 15 significant male mating success associations (q‐value < 0.1), and interestingly, we detected a nonrandom pattern in the relationship between allele frequency and direction of effect on male mating success. The minor‐frequency allele usually reduced male mating success, suggesting a positive association between male mating success and total fitness at this locus.     

Patterns of genetic variation and covariation in ejaculate traits reveal potential evolutionary constraints in guppies

Ejaculates comprise multiple and potentially interacting traits that determine male fertility and sperm competitiveness. Consequently, selection on these traits is likely to be intense, but the efficacy of selection will depend critically on patterns of genetic variation and covariation underlying their expression. In this study, I provide a prospective quantitative genetic analysis of ejaculate traits in the guppy Poecilia reticulata, a highly promiscuous live-bearing fish. I used a standard paternal half-sibling breeding design to characterize patterns of genetic (co)variation in components of sperm length and in vitro sperm performance. All traits exhibited high levels of phenotypic and additive genetic variation, and in several cases, patterns of genetic variation was consistent with Y-linkage. There were also highly significant negative genetic correlations between the various measures of sperm length and sperm performance. In particular, the length of the sperm's midpiece was strongly, negatively and genetically correlated with sperm's swimming velocity-an important determinant of sperm competitiveness in this and other species. Other components of sperm length, including the flagellum and head, were independently and negatively genetically correlated with the proportion of live sperm in the ejaculate (sperm viability). Whether these relationships represent evolutionary trade-offs depends on the precise relationships between these traits and competitive fertilization rates, which have yet to be fully resolved in this (and indeed most) species. Nevertheless, these prospective analyses point to potential constraints on ejaculate evolution and may explain the high level of phenotypic variability in ejaculate traits in this species.     

Estimators for QST and coalescence times

Comparisons of to can provide insights into the evolutionary processes that lead to differentiation, or lack thereof, among the phenotypes of different groups (e.g., populations, species), and these comparisons have been performed on a variety of taxa, including humans. Here, I show that for neutrally evolving (i.e., by genetic drift, mutation, and gene flow alone) quantitative characters, the two commonly used estimators have somewhat different interpretations in terms of coalescence times, particularly when the number of groups that have been sampled is small. A similar situation occurs for estimators. Consequently, when observations come from only a small number of groups, which is not an unusual situation, it is important to match estimators appropriately when comparing to .     

Macronutrient intake regulates sexual conflict in decorated crickets

Sexual conflict results in a diversity of sex‐specific adaptations, including chemical additions to ejaculates. Male decorated crickets (Gryllodes sigillatus) produce a gelatinous nuptial gift (the spermatophylax) that varies in size and free amino acid composition, which influences a female's willingness to fully consume this gift. Complete consumption of this gift maximizes sperm transfer through increased retention of the sperm‐containing ampulla, but hinders post‐copulatory mate choice. Here, we examine the effects of protein (P) and carbohydrate (C) intake on the weight and amino acid composition of the spermatophylax that describes its gustatory appeal to the female, as well as the ability of this gift to regulate sexual conflict via ampulla attachment time. Nutrient intake had similar effects on the expression of these traits with each maximized at a high intake of nutrients with a P : C ratio of 1 : 1.3. Under dietary choice, males actively regulated their nutrient intake but this regulation did not coincide with the peak of the nutritional landscape for any trait. Our results therefore demonstrate that a balanced intake of nutrients is central to regulating sexual conflict in G. sigillatus, but males are constrained from reaching the optima needed to bias the outcome of this conflict in their favour.     

A composite method for mapping quantitative trait loci without interference of female achiasmatic and gender effects in silkworm,Bombyx mori

The silkworm, Bombyx mori, is an economically important insect that was domesticated more than 5000 years ago. Its major economic traits focused on by breeders are quantitative traits, and an accurate and efficient QTL mapping method is necessary to explore their genetic architecture. However, current widely used QTL mapping models are not well suited for silkworm because they ignore female achiasmate and gender effects. In this study, we propose a composite method combining rational population selection and special mapping methods to map QTL in silkworm. By determining QTL for cocoon shell weight (CSW), we demonstrated the effectiveness of this method. In the CSW mapping process, only 56 markers were used and five loci or chromosomes were detected, more than in previous studies. Additionally, loci on chromosomes 1 and 11 dominated and accounted for 35.10% and 15.03% of the phenotypic variance respectively. Unlike previous studies, epistasis was detected between loci on chromosomes 11 and 22. These mapping results demonstrate the power and convenience of this method for QTL mapping in silkworm, and this method may inspire the development of similar approaches for other species with special genetic characteristics.     

Distribution of genetic variation underlying adult migration timing in steelhead of the Columbia River basin

Fish migrations are energetically costly, especially when moving between freshwater and saltwater, but are a viable strategy for Pacific salmon and trout (Oncorhynchus spp.) due to the advantageous resources available at various life stages. Anadromous steelhead (O. mykiss) migrate vast distances and exhibit variation for adult migration phenotypes that have a genetic basis at candidate genes known as greb1L and rock1. We examined the distribution of genetic variation at 13 candidate markers spanning greb1L, intergenic, and rock1 regions versus 226 neutral markers for 113 populations (n = 9,471) of steelhead from inland and coastal lineages in the Columbia River. Patterns of population structure with neutral markers reflected genetic similarity by geographic region as demonstrated in previous studies, but candidate markers clustered populations by genetic variation associated with adult migration timing. Mature alleles for late migration had the highest frequency overall in steelhead populations throughout the Columbia River, with only 9 of 113 populations that had a higher frequency of premature alleles for early migration. While a single haplotype block was evident for the coastal lineage, we identified multiple haplotype blocks for the inland lineage. The inland lineage had one haplotype block that corresponded to candidate markers within the greb1L gene and immediately upstream in the intergenic region, and the second block only contained candidate markers from the intergenic region. Haplotype frequencies had similar patterns of geographic distribution as single markers, but there were distinct differences in frequency between the two haplotype blocks for the inland lineage. This may represent multiple recombination events that differed between lineages where phenotypic differences exist between freshwater entry versus arrival timing as indicated by Micheletti et al. (2018a). Redundancy analyses were used to model environmental effects on allelic frequencies of candidate markers, and significant variables were migration distance, temperature, isothermality, and annual precipitation. This study improves our understanding of the spatial distribution of genetic variation underlying adult migration timing in steelhead as well as associated environmental factors and has direct conservation and management implications.