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How phenotypic diversity originates and persists within populations are classic puzzles in evolutionary biology. While balanced polymorphisms segregate within many species, it remains rare for both the genetic basis and the selective forces to be known, leading to an incomplete understanding of many classes of traits under balancing selection. Here, we uncover the genetic architecture of a balanced sexual mimicry polymorphism and identify behavioral mechanisms that may be involved in its maintenance in the swordtail fish Xiphophorus birchmanni. We find that ∼40% of X. birchmanni males develop a "false gravid spot," a melanic pigmentation pattern that mimics the "pregnancy spot" associated with sexual maturity in female live-bearing fish. Using genome-wide association mapping, we detect a single intergenic region associated with variation in the false gravid spot phenotype, which is upstream of kitlga, a melanophore patterning gene. By performing long-read sequencing within and across populations, we identify complex structural rearrangements between alternate alleles at this locus. The false gravid spot haplotype drives increased allele-specific expression of kitlga, which provides a mechanistic explanation for the increased melanophore abundance that causes the spot. By studying social interactions in the laboratory and in nature, we find that males with the false gravid spot experience less aggression; however, they also receive increased attention from other males and are disdained by females. These behavioral interactions may contribute to the maintenance of this phenotypic polymorphism in natural populations. We speculate that structural variants affecting gene regulation may be an underappreciated driver of balanced polymorphisms across diverse species., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2024 The Author(s). Published by Elsevier Inc. All rights reserved.)

Family-based genome-wide association studies (GWASs) are often claimed to provide an unbiased estimate of the average causal effects (or average treatment effects; ATEs) of alleles, on the basis of an analogy between the random transmission of alleles from parents to children and a randomized controlled trial. We show that this claim does not hold in general. Because Mendelian segregation only randomizes alleles among children of heterozygotes, the effects of alleles in the children of homozygotes are not observable. This feature will matter if an allele has different average effects in the children of homozygotes and heterozygotes, as can arise in the presence of gene-by-environment interactions, gene-by-gene interactions, or differences in linkage disequilibrium patterns. At a single locus, family-based GWAS can be thought of as providing an unbiased estimate of the average effect in the children of heterozygotes (i.e., a local average treatment effect; LATE). This interpretation does not extend to polygenic scores (PGSs), however, because different sets of SNPs are heterozygous in each family. Therefore, other than under specific conditions, the within-family regression slope of a PGS cannot be assumed to provide an unbiased estimate of the LATE for any subset or weighted average of families. In practice, the potential biases of a family-based GWAS are likely smaller than those that can arise from confounding in a standard, population-based GWAS, and so family studies remain important for the dissection of genetic contributions to phenotypic variation. Nonetheless, their causal interpretation is less straightforward than has been widely appreciated., Competing Interests: Competing interests statement:The authors declare no competing interest.

Over the past 2 decades, biologists have come to appreciate that hybridization, or genetic exchange between distinct lineages, is remarkably common-not just in particular lineages but in taxonomic groups across the tree of life. As a result, the genomes of many modern species harbor regions inherited from related species. This observation has raised fundamental questions about the degree to which the genomic outcomes of hybridization are repeatable and the degree to which natural selection drives such repeatability. However, a lack of appropriate systems to answer these questions has limited empirical progress in this area. Here, we leverage independently formed hybrid populations between the swordtail fish Xiphophorus birchmanni and X. cortezi to address this fundamental question. We find that local ancestry in one hybrid population is remarkably predictive of local ancestry in another, demographically independent hybrid population. Applying newly developed methods, we can attribute much of this repeatability to strong selection in the earliest generations after initial hybridization. We complement these analyses with time-series data that demonstrates that ancestry at regions under selection has remained stable over the past approximately 40 generations of evolution. Finally, we compare our results to the well-studied X. birchmanni × X. malinche hybrid populations and conclude that deeper evolutionary divergence has resulted in stronger selection and higher repeatability in patterns of local ancestry in hybrids between X. birchmanni and X. cortezi., Competing Interests: The authors have declared that no competing interests exist., (Copyright: © 2024 Langdon et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.)

Species range sizes and realized niche breadths vary tremendously. Understanding the source of this variation has been a long-term aim in evolutionary ecology and is a major tool in efforts to ameliorate the impacts of changing climates on species distributions. Species ranges that span a large climatic envelope can be achieved by a collection of specialized genotypes locally adapted to a small range of conditions, by genotypes with stable fitness across variable environments, or a combination of these factors. We asked whether fitness expressed along a key niche axis, water availability, could explain a species' realized niche breadth, its geographic range and climate breadth, in 11 species from a clade of jewelflowers whose range sizes vary by two orders of magnitude. Specifically, we explored whether the range size of a species was related to the ability of genotypes (maternal families) to maintain fitness across a range of experimental water availabilities based on 30-year historical field precipitation regimes. We operationally characterized fitness homeostasis through the coefficient of variation in fitness of a genotype (family) across the experimental water gradient. We found that species with genotypes that had high fitness homeostasis, low variation in fitness over our treatments, had larger climatic niche breadth and geographic range in their field distributions. The result was robust to alternate measures of fitness homeostasis. Our results show that the fitness homeostasis of genotypes can be a major factor contributing to niche breadth and range size in this clade. Fitness homeostasis can buffer species from loss of genetic diversity and under changing climates, provides time for adaptation to future conditions., (© 2022 The Ecological Society of America. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.)

A reply to Harden's response to Coop and Przeworski (2022)., (© 2022 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.)

Given the many small-effect loci uncovered by genome-wide association studies (GWAS), polygenic scores have become central to genomic medicine, and have found application in diverse settings including evolutionary studies of adaptation. Despite their promise, polygenic scores have been found to suffer from limited portability across human populations. This at first seems in conflict with the observation that most common genetic variation is shared among populations. We investigate one potential cause of this discrepancy: stabilizing selection on complex traits. Counterintuitively, while stabilizing selection constrains phenotypic evolution, it accelerates the loss and fixation of alleles underlying trait variation within populations (GWAS loci). Thus even when populations share an optimum phenotype, stabilizing selection erodes the variance contributed by their shared GWAS loci, such that predictions from GWAS in one population explain less of the phenotypic variation in another. We develop theory to quantify how stabilizing selection is expected to reduce the prediction accuracy of polygenic scores in populations not represented in GWAS samples. In addition, we find that polygenic scores can substantially overstate average genetic differences of phenotypes among populations. We emphasize stabilizing selection around a common optimum as a useful null model to connect patterns of allele frequency and polygenic score differentiation. This article is part of the theme issue 'Celebrating 50 years since Lewontin's apportionment of human diversity'.

Hybridization is among the evolutionary mechanisms most frequently hypothesized to drive the success of invasive species, in part because hybrids are common in invasive populations. One explanation for this pattern is that biological invasions coincide with a change in selection pressures that limit hybridization in the native range. To investigate this possibility, we studied the introduction of the brown anole ( Anolis sagrei ) in the southeastern United States. We find that native populations are highly genetically structured. In contrast, all invasive populations show evidence of hybridization among native-range lineages. Temporal sampling in the invasive range spanning 15 y showed that invasive genetic structure has stabilized, indicating that large-scale contemporary gene flow is limited among invasive populations and that hybrid ancestry is maintained. Additionally, our results are consistent with hybrid persistence in invasive populations resulting from changes in natural selection that occurred during invasion. Specifically, we identify a large-effect X chromosome locus associated with variation in limb length, a well-known adaptive trait in anoles, and show that this locus is often under selection in the native range, but rarely so in the invasive range. Moreover, we find that the effect size of alleles at this locus on limb length is much reduced in hybrids among divergent lineages, consistent with epistatic interactions. Thus, in the native range, epistasis manifested in hybrids can strengthen extrinsic postmating isolation. Together, our findings show how a change in natural selection can contribute to an increase in hybridization in invasive populations., Competing Interests: The authors declare no competing interest.

Transposable elements (TEs) constitute the majority of flowering plant DNA, reflecting their tremendous success in subverting, avoiding, and surviving the defenses of their host genomes to ensure their selfish replication. More than 85% of the sequence of the maize genome can be ascribed to past transposition, providing a major contribution to the structure of the genome. Evidence from individual loci has informed our understanding of how transposition has shaped the genome, and a number of individual TE insertions have been causally linked to dramatic phenotypic changes. Genome-wide analyses in maize and other taxa have frequently represented TEs as a relatively homogeneous class of fragmentary relics of past transposition, obscuring their evolutionary history and interaction with their host genome. Using an updated annotation of structurally intact TEs in the maize reference genome, we investigate the family-level dynamics of TEs in maize. Integrating a variety of data, from descriptors of individual TEs like coding capacity, expression, and methylation, as well as similar features of the sequence they inserted into, we model the relationship between attributes of the genomic environment and the survival of TE copies and families. In contrast to the wholesale relegation of all TEs to a single category of junk DNA, these differences reveal a diversity of survival strategies of TE families. Together these generate a rich ecology of the genome, with each TE family representing the evolution of a distinct ecological niche. We conclude that while the impact of transposition is highly family- and context-dependent, a family-level understanding of the ecology of TEs in the genome can refine our ability to predict the role of TEs in generating genetic and phenotypic diversity., Competing Interests: The authors have declared that no competing interests exist.

One of the most useful models in population genetics is that of a selective sweep and the consequent hitch-hiking of linked neutral alleles. While variations on this model typically assume constant population size, many instances of strong selection and rapid adaptation in nature may co-occur with complex demography. Here, we extend the hitch-hiking model to evolutionary rescue, where adaptation and demography not only co-occur but are intimately entwined. Our results show how this feedback between demography and evolution determines-and restricts-the genetic signatures of evolutionary rescue, and how these differ from the signatures of sweeps in populations of constant size. In particular, we find rescue to harden sweeps from standing variance or new mutation (but not from migration), reduce genetic diversity both at the selected site and genome-wide, and increase the range of observed Tajima's D values. For a given initial rate of population decline, the feedback between demography and evolution makes all of these differences more dramatic under weaker selection, where bottlenecks are prolonged. Nevertheless, it is likely difficult to infer the co-incident timing of the sweep and bottleneck from these simple signatures, never mind a feedback between them. Temporal samples spanning contemporary rescue events may offer one way forward., (Copyright © 2020 by the Genetics Society of America.)

Understanding the population genetic consequences of declining population size is important for conserving the many species worldwide facing severe decline [1]. Thorough empirical studies on the impacts of population reduction at a genome-wide scale in the wild are scarce because they demand huge field and laboratory investments [1, 2]. Previous studies have demonstrated the importance of gene flow in introducing genetic variation to small populations [3], but few have documented both genetic and fitness consequences of decreased immigration through time in a natural population [4-6]. Here we assess temporal variation in gene flow, inbreeding, and fitness using longitudinal genomic, demographic, and phenotypic data from a long-studied population of federally Threatened Florida scrub-jays (Aphelocoma coerulescens). We exhaustively sampled and genotyped the study population over two decades, providing one of the most detailed longitudinal investigations of genetics in a wild animal population to date. Immigrants were less heterozygous than residents but still introduced genetic variation into our study population. Owing to regional population declines, immigration into the study population declined from 1995-2013, resulting in increased levels of inbreeding and reduced fitness via inbreeding depression, even as the population remained demographically stable. Our results show that, contrary to conventional wisdom, small peripheral populations that already have undergone a genetic bottleneck may play a vital role in preserving genetic diversity of larger and seemingly stable populations. These findings underscore the importance of investing in the persistence of small populations and maintaining population connectivity in conservation of fragmented species., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

The butterfly tribe Melitaeini [Nymphalidae] contains numerous species that have been the subjects of a wide range of biological studies. Despite numerous taxonomic revisions, many of the evolutionary relationships within the tribe remain unresolved. Utilizing mitochondrial and nuclear gene regions, we produced a time-calibrated phylogenetic hypothesis for 222 exemplars comprising at least 178 different species and 21 of the 22 described genera, making this the most complete phylogeny of the tribe to date. Our results suggest that four well-supported clades corresponding to the subtribes Euphydryina, Chlosynina, Melitaeina, and Phyciodina exist within the tribe. This analysis is also represents the most complete phylogenetic analysis of the Chlosynina to date, and includes several genera and species that have been previously excluded from published phylogenies of this group., (Copyright © 2014 Elsevier Inc. All rights reserved.)

Transposable elements (TEs) are considered to be genomic parasites and their interactions with their hosts have been likened to the coevolution between host and other nongenomic, horizontally transferred pathogens. TE families, however, are vertically inherited as integral segments of the nuclear genome. This transmission strategy has been suggested to weaken the selective benefits of host alleles repressing the transposition of specific TE variants. On the other hand, the elevated rates of TE transposition and high incidences of deleterious mutations observed during the rare cases of horizontal transfers of TE families between species could create at least a transient process analogous to the influence of horizontally transmitted pathogens. Here, we formally address this analogy, using empirical and theoretical analysis to specify the mechanism of how host-TE interactions may drive the evolution of host genes. We found that host TE-interacting genes actually have more pervasive evidence of adaptive evolution than immunity genes that interact with nongenomic pathogens in Drosophila. Yet, both our theoretical modeling and empirical observations comparing Drosophila melanogaster populations before and after the horizontal transfer of P elements, which invaded D. melanogaster early last century, demonstrated that horizontally transferred TEs have only a limited influence on host TE-interacting genes. We propose that the more prevalent and constant interaction with multiple vertically transmitted TE families may instead be the main force driving the fast evolution of TE-interacting genes, which is fundamentally different from the gene-for-gene interaction of host-pathogen coevolution.

Theories to explain the prevalence of sex and recombination have long been a central theme of evolutionary biology. Yet despite decades of attention dedicated to the evolution of sex and recombination, the widespread pattern of sex differences in the recombination rate is not well understood and has received relatively little theoretical attention. Here, we argue that female meiotic drivers--alleles that increase in frequency by exploiting the asymmetric cell division of oogenesis--present a potent selective pressure favoring the modification of the female recombination rate. Because recombination plays a central role in shaping patterns of variation within and among dyads, modifiers of the female recombination rate can function as potent suppressors or enhancers of female meiotic drive. We show that when female recombination modifiers are unlinked to female drivers, recombination modifiers that suppress harmful female drive can spread. By contrast, a recombination modifier tightly linked to a driver can increase in frequency by enhancing female drive. Our results predict that rapidly evolving female recombination rates, particularly around centromeres, should be a common outcome of meiotic drive. We discuss how selection to modify the efficacy of meiotic drive may contribute to commonly observed patterns of sex differences in recombination.

Adaptive genetic differentiation and adaptive phenotypic plasticity can increase the fitness of plant lineages in heterogeneous environments. We examine the relative importance of genetic differentiation and plasticity in determining the fitness of the annual plant, Erodium cicutarium, in a serpentine grassland in California. Previous work demonstrated that the serpentine sites within this mosaic display stronger dispersal-scale heterogeneity than nonserpentine sites. We conducted a reciprocal transplant experiment among six sites to characterize selection on plasticity expressed by 180 full-sibling families in response to natural environmental heterogeneity across these sites. Multivariate axes of environmental variation were constructed using a principal components analysis of soil chemistry data collected at every experimental block. Simple linear regressions were used to characterize the intercept, and slope (linear and curvilinear) of reaction norms for each full-sibling family in response to each axis of environmental variation. Multiple linear regression analyses revealed significant selection on trait means and slopes of reaction norms. Multivariate analyses of variance demonstrated genetic differentiation between serpentine and nonserpentine lineages in the expression of plasticity in response to three of the five axes of environmental variation considered. In all but one case, serpentine genotypes expressed a stronger adaptive plastic response than nonserpentine genotypes., (© 2010 The Author(s). Journal compilation © 2010 The Society for the Study of Evolution.)

PhyLIS is a free GNU/Linux distribution that is designed to provide a simple, standardized platform for phylogenetic and phyloinformatic analysis. The operating system incorporates most commonly used phylogenetic software, which has been pre-compiled and pre-configured, allowing for straightforward application of phylogenetic methods and development of phyloinformatic pipelines in a stable Linux environment. The software is distributed as a live CD and can be installed directly or run from the CD without making changes to the computer. PhyLIS is available for free at http://www.eve.ucdavis.edu/rcthomson/phylis/.

When the morphological diversity of a clade of species is quantified as the among-species variance in morphology, that diversity is a joint consequence of the phylogenetic structure of the clade (i.e., temporal pattern of speciation events) and the rates of change in the morphological traits of interest. Extrinsic factors have previously been linked to variation in the rate of morphological change among clades. Here, we ask whether species co-occurrence is positively correlated with the rate of change in several ecologically relevant morphological characters using the North American freshwater fish clade Percina (Teleostei: Etheostomatinae). We constructed a time-calibrated phylogenetic tree of Percina from mtDNA sequence data, gathered data on eight morphological characters from 37 species, used a principal components analysis to identify the primary axes of morphological variation, and analyzed 16,094 collection records to estimate species co-occurrence. We then calculated standardized independent contrasts (SIC) of the morphological traits (rate of change) at each node, estimated ancestral species co-occurrence, and quantified the correlation between species co-occurrence and rate of morphological change. We find that morphology changes more quickly when co-occurrence is greater in Percina. Our results provide strong evidence that co-occurrence among close relatives is linked to the morphological diversification of this clade.

Studies examining plant distribution patterns across environmental gradients have generally focused on perennial-dominated systems, and we know relatively little about the processes structuring annual communities. Here, the ecological factors determining local distribution patterns of five dominant annual species distributed across micro-topographic gradients in ephemeral California wetlands are examined. Over two growing seasons in three vernal pools, patterns of inundation and above-ground biomass were characterized across the microtopographic gradient, population boundaries for five dominant species were documented and a reciprocal transplant experiment and neighbor removal treatment were conducted to test the relative effects of within-pool elevation, competition and seed dispersal on plant performance. Despite large differences in inundation time between growing seasons, above-ground biomass and the elevation of population boundaries remained consistent. The predicted 'optimal' depth for each species shifted between years, but competition and recruitment limitation restricted species' abilities to track these conditions. The distributions of the focal taxa are primarily driven by differential responses to environmental conditions associated with different microtopographic positions along pool inundation gradients, and are reinforced by competition and dispersal constraints. The relative importance of competition, other environmental factors and dispersal patterns appear to contrast with results obtained in systems dominated by perennial plants.