Males and females share many traits that have a common genetic basis; however, selection on these traits often differs between the sexes, leading to sexual conflict. Under such sexual antagonism, theory predicts the evolution of genetic architectures that resolve this sexual conflict. Yet, despite intense theoretical and empirical interest, the specific loci underlying sexually antagonistic phenotypes have rarely been identified, limiting our understanding of how sexual conflict impacts genome evolution and the maintenance of genetic diversity. Here we identify a large effect locus controlling age at maturity in Atlantic salmon (Salmo salar), an important fitness trait in which selection favours earlier maturation in males than females, and show it is a clear example of sex-dependent dominance that reduces intralocus sexual conflict and maintains adaptive variation in wild populations. Using high-density single nucleotide polymorphism data across 57 wild populations and whole genome re-sequencing, we find that the vestigial-like family member 3 gene (VGLL3) exhibits sex-dependent dominance in salmon, promoting earlier and later maturation in males and females, respectively. VGLL3, an adiposity regulator associated with size and age at maturity in humans, explained 39% of phenotypic variation, an unexpectedly large proportion for what is usually considered a highly polygenic trait. Such large effects are predicted under balancing selection from either sexually antagonistic or spatially varying selection. Our results provide the first empirical example of dominance reversal allowing greater optimization of phenotypes within each sex, contributing to the resolution of sexual conflict in a major and widespread evolutionary trade-off between age and size at maturity. They also provide key empirical evidence for how variation in reproductive strategies can be maintained over large geographical scales. We anticipate these findings will have a substantial impact on population management in a range of harvested species where trends towards earlier maturation have been observed.
Morphological traits often covary within and among species according to simple power laws referred to as allometry. Such allometric relationships may result from common growth regulation, and this has given rise to the hypothesis that allometric exponents may have low evolvability and constrain trait evolution. We formalize hypotheses for how allometry may constrain morphological trait evolution across taxa, and test these using more than 300 empirical estimates of static (within-species) allometric relations of animal morphological traits. Although we find evidence for evolutionary changes in allometric parameters on million-year, cross-species time scales, there is limited evidence for microevolutionary changes in allometric slopes. Accordingly, we find that static allometries often predict evolutionary allometries on the subspecies level, but less so across species. Although there is a large body of work on allometry in a broad sense that includes all kinds of morphological trait-size relationships, we found relatively little information about the evolution of allometry in the narrow sense of a power relationship. Despite the many claims of microevolutionary changes of static allometries in the literature, hardly any of these apply to narrow-sense allometry, and we argue that the hypothesis of strongly constrained static allometric slopes remains viable. K E Y W O R D S :Adaptation, evolutionary constraint, microevolution, macroevolution, ontogenetic allometry, static allometry.
23Allometry refers to the power-law relationship that often occurs between body parts and total 24 body size. Whether measured during growth (ontogenetic allometry), among individuals at 25 similar developmental stage (static allometry) or among populations or species (evolutionary 26 allometry), allometric relationships are often surprisingly tight, and relatively invariant. 27Consequently, it has been suggested that allometry could constrain phenotypic evolution, that 28 is, force evolving species along fixed trajectories. Alternatively allometric relationship may 29 result from selection. Despite nearly a century of active research on allometry, distinguishing 30 between these two alternatives remains difficult partly due to the use of a broad sense 31 definition of allometry where the meaning of relative growth was lost. Focusing on the 32 original narrow-sense definition of allometry, we review evidence for and against the 33 "allometry as a constraint" hypothesis. Although the low evolvability of the static allometric 34 slopes observed in some studies suggests a possible constraining effect of this parameter on 35 phenotypic evolution, the nearly complete absence of knowledge about selection on allometry 36 prevents any firm conclusion. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 Introduction 42Allometry is the study of the relationship between body size and other organismal traits. 43Allometry is important because variation in a wide variety of morphological, physiological 44 and life history traits are highly correlated with organism size [1,2,3]. These relationships 45 generate intuitive hypotheses for understanding trait variation; for example, the fact that 46 humans are larger than mice can be used to explain why the basal metabolic rate of a human 47 is much higher than the basal metabolic rate of a mouse. In most cases, traits show a non-48 linear relationship with size that is accurately captured by a power relationship of the form z = 49, where the trait value is z, the organism size is x, and a and b are parameters of the 50 relationship. If b = 1, the relationship between the trait and size is linear, a condition referred 51 to as isometry. When b ≠ 1, the relationship is non-linear on the arithmetic scale. For 52 example, the basal metabolic rate in mammals scales with body mass with a coefficient b ≈ 53 0.71 [4]; as a result, for every unit increase in mass, a larger organism will have a smaller 54 increase in basal metabolic rate than a smaller organism. Consequently, humans have a basal 55 metabolic rate 5 to 10 times smaller than a mouse when corrected for body size. The ubiquity 56 of these power-law relationships has led biologists to refer to them as allometric relationships. 57Analyzed on log-transformed data these relationships become linear: log(z) = log(a) + 58 b×log(x), where log(a) and b re...
Integration and modularity refer to the patterns and processes of trait interaction and independence. Both terms have complex histories with respect to both conceptualization and quantification, resulting in a plethora of integration indices in use. We review briefly the divergent definitions, uses and measures of integration and modularity and make conceptual links to allometry. We also discuss how integration and modularity might evolve. Although integration is generally thought to be generated and maintained by correlational selection, theoretical considerations suggest the relationship is not straightforward. We caution here against uncontrolled comparisons of indices across studies. In the absence of controls for trait number, dimensionality, homology, development and function, it is difficult, or even impossible, to compare integration indices across organisms or traits. We suggest that care be invested in relating measurement to underlying theory or hypotheses, and that summative, theory-free descriptors of integration generally be avoided. The papers that follow in this Theme Issue illustrate the diversity of approaches to studying integration and modularity, highlighting strengths and pitfalls that await researchers investigating integration in plants and animals.
Mutation enables evolution, but the idea that adaptation is also shaped by mutational variation is controversial. Simple evolutionary hypotheses predict such a relationship if the supply of mutations constrains evolution, but it is not clear that constraints exist, and, even if they do, they may be overcome by long-term natural selection. Quantification of the relationship between mutation and phenotypic divergence among species will help to resolve these issues. Here we use precise data on over 50,000 Drosophilid fly wings to demonstrate unexpectedly strong positive relationships between variation produced by mutation, standing genetic variation, and the rate of evolution over the last 40 million years. Our results are inconsistent with simple constraint hypotheses because the rate of evolution is very low relative to what both mutational and standing variation could allow. In principle, the constraint hypothesis could be rescued if the vast majority of mutations are so deleterious that they cannot contribute to evolution, but this also requires the implausible assumption that deleterious mutations have the same pattern of effects as potentially advantageous ones. Our evidence for a strong relationship between mutation and divergence in a slowly evolving structure challenges the existing models of mutation in evolution.
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