Integrating genomics and multivariate evolutionary quantitative genetics: a case study of constraints on sexual selection in Drosophila serrata

In evolutionary quantitative genetics, the genetic variance–covariance matrix, G , and the vector of directional selection gradients, β , are key parameters for predicting multivariate selection responses and genetic constraints. Historically, investigations of G and β have not overlapped with those dissecting the genetic basis of quantitative traits. Thus, it remains unknown whether these parameters reflect pleiotropic effects at individual loci. Here, we integrate multivariate genome-wide association study (GWAS) with G and β estimation in a well-studied system of multivariate constraint: sexual selection on male cuticular hydrocarbons (CHCs) in Drosophila serrata . In a panel of wild-derived re-sequenced lines, we augment genome-based restricted maximum likelihood to estimate G alongside multivariate single nucleotide polymorphism (SNP) effects, detecting 532 significant associations from 1 652 276 SNPs. Constraint was evident, with β lying in a direction of G with low evolvability. Interestingly, minor frequency alleles typically increased male CHC-attractiveness suggesting opposing natural selection on β . SNP effects were significantly misaligned with the major eigenvector of G , g max , but well aligned to the second and third eigenvectors g 2 and g 3 . We discuss potential factors leading to these varied results including multivariate stabilizing selection and mutational bias. Our framework may be useful as researchers increasingly access genomic methods to study multivariate selection responses in wild populations.

Integrating genomics and multivariate evolutionary quantitative genetics: A case study of multivariate constraints on sexual selection in Drosophila serrata

In evolutionary quantitative genetics, the genetic variance-covariance matrix, G, and the vector of directional selection gradients, β , are key parameters for predicting multivariate selection responses and genetic constraints. Historically, investigations of G and β have not overlapped with those dissecting the genetic basis of quantitative traits. Thus, it remains unknown whether these parameters reflect pleiotropic effects at individual loci. Here, we integrate multivariate GWAS with G and β estimation in a well-studied system of multivariate constraint; sexual selection on male cuticular hydrocarbons (CHCs) in Drosophila serrata. In a panel of wild-derived resequenced lines, we augment genome-based REML, (GREML) to estimate G alongside multivariate SNP effects, detecting 532 significant associations from 1,652,276 SNPs. Constraint was evident, with β lying in a direction of G with low evolvability. Interestingly, minor frequency alleles typically increased male CHC-attractiveness suggesting opposing natural selection on β. SNP effects were significantly misaligned with the major eigenvector of G, gmax, but well aligned to the second and third eigenvectors g2 and g3. We discuss potential factors leading to these varied results including multivariate stabilising selection and mutational bias. Our framework may be useful as researchers increasingly access genomic methods to study multivariate selection responses in wild populations.

Senescence: why and where selection gradients might not decline with age

Patterns of ageing across the tree of life are much more diverse than previously thought. Yet, we still do not adequately understand how, why and where across the tree of life a particular pattern of ageing will evolve. An ability to predict ageing patterns requires a firmer understanding of how and why different ecological and evolutionary factors alter the sensitivity of fitness to age-related changes in mortality and reproduction. From this understanding, we can ask why and where selection gradients might not decline with age. Here, we begin by summarizing the recent breadth of literature that is unearthing, empirically and theoretically, the mechanisms that drive variation in patters of senescence. We focus on the relevance of two key parameters, population structure and reproductive value, as key to understanding selection gradients, and therefore senescence. We discuss how growth form, individual trade-offs, stage structure and social interactions may all facilitate differing distributions of these two key parameters than those predicted by classical theory. We argue that these four key aspects can help us understand why patterns of negligible and negative senescence can actually be explained under the same evolutionary framework as classical senescence.

Pollinator-Mediated Selection on Floral Traits in the Arctic Plant Parrya nudicaulis (Brassicaceae)

The evolution of floral traits is largely attributed to pollinator-mediated selection; however, the importance of pollinators as selective agents in pollen-limited environments is poorly resolved. In pollen-limited arctic and subarctic regions, selection is expected to either favor floral traits that increase pollinator attraction or promote reproductive assurance through selfing. We quantified phenotypic selection on floral traits in two arctic and two subarctic populations of Parrya nudicaulis. Additionally, we measured selection in plants in both open-pollination and pollen-augmentation treatments to estimate selection imposed by pollinators in one population. Seed production was found to be limited by pollen availability and strong directional selection on flower number was observed. We did not detect consistently greater magnitudes of selection on floral traits in the arctic relative to the subarctic populations. Directional selection for more pigmented flowers in one arctic population was observed however. In some populations, selection on flower color was found to interact with other traits. We did not detect consistently stronger selection gradients across all traits for plants exposed to pollinator selection relative to those in the pollen-augmentation treatment; however directional selection tended to be higher for some floral traits in open-pollinated plants.

Constrained flexibility of parental cooperation limits evolutionary responses to harsh conditions

Parental care is predicted to evolve to mitigate harsh environments, thus adaptive plasticity of care may be an important response to climate change. In biparental species, fitness costs may be reduced with plasticity of behavior among partners. We investigated this prediction with the burying beetle, Nicrophorus orbicollis, by exposing them to contrasting benign and harsh thermal environments. We found strong fitness costs under the harsh environment, but rather than select for more care, visualized selection was stabilizing. Examining different components of care revealed positive directional selection gradients for direct care and strong stabilizing selection gradients for indirect care, resulting in constrained evolutionary responses. Further, because males and females did not coordinate their investments, the potential for adaptive plasticity was not enhanced under biparental care. Females cared at capacity with or without male partners, while males with partners reduced direct care but maintained indirect care levels. Decision rules were not altered in different environments, suggesting no shift from sexual conflict to cooperation. We suggest that the potential for parenting to ameliorate the effects of our climate crisis may depend on the sex-specific evolutionary drivers of parental care, and that this may be best reflected in components of care.

A Synthesis of Game Theory and Quantitative Genetic Models of Social Evolution

Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory, and in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates.

Life-history evolution of class-structured populations in fluctuating environments

What is the influence of periodic environmental fluctuations on life-history evolution? We present a general theoretical framework to understand and predict the long-term evolution of life-history traits under a broad range of ecological scenarios. Indeed, this analysis yields time-varying selection gradients that help dissect the influence of the fluctuations of the environment on the competitive ability of a specific life-history mutation. We use this framework to analyse the evolution of key life-history traits of pathogens, such as transmission and virulence. These examples reveal how periodic fluctuations of the environment can affect the evolution of pathogens, and illustrate the usefulness and broad applicability of this new approach.

Measuring Pre- and Post-Copulatory Sexual Selection and Their Interaction in Socially Monogamous Species with Extra-Pair Paternity

When females copulate with multiple males, pre- and post-copulatory sexual selection may interact synergistically or in opposition. Studying this interaction in wild populations is complex and potentially biased, because copulation and fertilization success are often inferred from offspring parentage rather than being directly measured. Here, I simulated 15 species of socially monogamous birds with varying levels of extra-pair paternity, where I could independently cause a male secondary sexual trait to improve copulation success, and a sperm trait to improve fertilization success. By varying the degree of correlation between the male and sperm traits, I show that several common statistical approaches, including univariate selection gradients and paired t-tests comparing extra-pair males to the within-pair males they cuckolded, can give highly biased results for sperm traits. These tests should therefore be avoided for sperm traits in socially monogamous species with extra-pair paternity, unless the sperm trait is known to be uncorrelated with male trait(s) impacting copulation success. In contrast, multivariate selection analysis and a regression of the proportion of extra-pair brood(s) sired on the sperm trait of the extra-pair male (including only broods where the male sired ≥1 extra-pair offspring) were unbiased, and appear likely to be unbiased under a broad range of conditions for this mating system. In addition, I investigated whether the occurrence of pre-copulatory selection impacted the strength of post-copulatory selection, and vice versa. I found no evidence of an interaction under the conditions simulated, where the male trait impacted only copulation success and the sperm trait impacted only fertilization success. Instead, direct selection on each trait was independent of whether the other trait was under selection. Although pre- and post-copulatory selection strength was independent, selection on the two traits was positively correlated across species because selection on both traits increased with the frequency of extra-pair copulations in these socially monogamous species.

Endocranial volume is variable and heritable, but not related to fitness, in a free-ranging primate

Large relative brain size is a defining characteristic of the order Primates. Arguably, this can be attributed to selection for behavioral aptitudes linked to a larger brain size. In order for selection of a trait to occur, the trait must vary, that variation must be heritable, and enhance fitness. In this study, we use a quantitative genetic approach to investigate the production and maintenance of variation in endocranial volume in a population of free-ranging rhesus macaques. We measured the endocranial volume and body mass proxies of 542 rhesus macaques from Cayo Santiago. We investigated variation in endocranial volume within and between sexes. Using a genetic pedigree, we estimated heritability of absolute and relative endocranial volume, and selection gradients of both traits as well as estimated body mass in the sample. Within this population, both absolute and relative endocranial volume display variation and sexual dimorphism. Both absolute and relative endocranial volume are highly heritable, but we found no evidence of selection on absolute or relative endocranial volume. These findings suggest that endocranial volume is not undergoing selection, or that we did not detect it because selection is neither linear nor quadratic, or that we lacked sufficient sample sizes to detect it.