Population genetic analyses often use summary statistics to describe patterns of genetic variation and provide insight into evolutionary processes. Among the most fundamental of these summary ...statistics are π and dXY, which are used to describe genetic diversity within and between populations, respectively. Here, we address a widespread issue in π and dXY calculation: systematic bias generated by missing data of various types. Many popular methods for calculating π and dXY operate on data encoded in the variant call format (VCF), which condenses genetic data by omitting invariant sites. When calculating π and dXY using a VCF, it is often implicitly assumed that missing genotypes (including those at sites not represented in the VCF) are homozygous for the reference allele. Here, we show how this assumption can result in substantial downward bias in estimates of π and dXY that is directly proportional to the amount of missing data. We discuss the pervasive nature and importance of this problem in population genetics, and introduce a user‐friendly UNIX command line utility, pixy, that solves this problem via an algorithm that generates unbiased estimates of π and dXY in the face of missing data. We compare pixy to existing methods using both simulated and empirical data, and show that pixy alone produces unbiased estimates of π and dXY regardless of the form or amount of missing data. In summary, our software solves a long‐standing problem in applied population genetics and highlights the importance of properly accounting for missing data in population genetic analyses.
Adaptation to new environments often occurs in the face of gene flow. Under these conditions, gene flow and recombination can impede adaptation by breaking down linkage disequilibrium between locally ...adapted alleles. Theory predicts that this decay can be halted or slowed if adaptive alleles are tightly linked in regions of low recombination, potentially favouring divergence and adaptive evolution in these regions over others. Here, we compiled a global genomic data set of over 1,300 individual threespine stickleback from 52 populations and compared the tendency for adaptive alleles to occur in regions of low recombination between populations that diverged with or without gene flow. In support of theory, we found that putatively adaptive alleles (FST and dXY outliers) tend to occur more often in regions of low recombination in populations where divergent selection and gene flow have jointly occurred. This result remained significant when we employed different genomic window sizes, controlled for the effects of mutation rate and gene density, controlled for overall genetic differentiation, varied the genetic map used to estimate recombination and used a continuous (rather than discrete) measure of geographic distance as proxy for gene flow/shared ancestry. We argue that our study provides the first statistical evidence that the interaction of gene flow and selection biases divergence toward regions of low recombination.
see also the Perspective by Marques
Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently ...renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper wasp Polistes fuscatus—a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps in P. fuscatus contain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures in P. fuscatus’ recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves.
Konopiński (2022) suggests that when averaging nucleotide diversity over a sequence, ignoring per‐site sample size variation (i.e., using an unweighted mean) offers an improvement in precision (lower ...variation) and accuracy (reduced bias). Here, I argue that preserving uncertainty due to variation in sample size is in line with best statistical practices, and that the increase in accuracy observed is not a general feature of the unweighted mean proposed by Konopiński (2022). As such, I conclude that the use of a weighted mean, as employed by (Korunes & Samuk, 2020), remains the preferred method for averaging nucleotide diversity over multiple sites.
Uncovering factors that shape variation in brain morphology remains a major challenge in evolutionary biology. Recently, it has been shown that brain size is positively associated with level of ...parental care behavior in various taxa. One explanation for this pattern is that the cognitive demands of performing complex parental care may require increased brain size. This idea is known as the parental brain hypothesis (PBH). We set out to test the predictions of this hypothesis in wild populations of threespine stickleback (Gasterosteus aculeatus). These fish are commonly known to exhibit (1) uniparental male care and (2) sexual dimorphism in brain size (males>females). To test the PBH, we took advantage of the existence of closely related populations of stickleback that display variation in parental care behavior: common marine threespine sticklebacks (uniparental male care) and white threespine sticklebacks (no care). To begin, we quantified genetic differentiation among two common populations and three white populations from Nova Scotia. We found overall low differentiation among populations, although FST was increased in between‐type comparisons. We then measured the brain weights of males and females from all five populations along with two additional common populations from British Columbia. We found that sexual dimorphism in brain size is reversed in white stickleback populations: males have smaller brains than females. Thus, while several alternatives need to be ruled out, the PBH appears to be a reasonable explanation for sexual dimorphism in brain size in threespine sticklebacks.
The parental brain hypothesis predicts that the sex performing parental care should have a larger brain than the non‐caring sex. We test this idea by examining brains of a unique white form of threespined stickleback that, unlike the common stickleback it co‐occurs with, does not perform paternal care. We found that male white sticklebacks have smaller relative brain weights than females – the opposite of the pattern in common sticklebacks.
Benthic and limnetic threespine stickleback (Gasterosteus aculeatus) are a classic example of ecological speciation. Behavioural and armour divergence between these species has been predicted to be ...the result of divergent selection driven in part by differential predation from cutthroat trout (Oncorhynchus clarki). To experimentally test this prediction, we reared split families of benthic–limnetic hybrids in the presence or absence of trout predation. Our results show that the presence of trout had little effect upon stickleback behaviour. We then compared performance in behavioural assays among stickleback that varied in armour to test if armour morphology correlates with behaviour. Our measurements revealed trait correlations between several behaviours and components of armour morphology. Trout predation did not result in an increased correlation between traits, therefore differential trout predation between benthics and limnetics is unlikely to be the cause of these correlations. The presence of trait correlations in advanced generation hybrids suggests that pleiotropy or linkage between genes underlying behaviour and armour morphology may be greater than previously appreciated.
How does adaptation manage to occur in the face of overwhelming gene flow? One popular idea is that the suppression of recombination, for example the fixation of a chromosomal inversion, can maintain ...linkage disequilibrium between groups of locally adapted alleles that would otherwise be degraded by gene flow. This idea has captured the imagination of many geneticists and evolutionary biologists, but we still have only a basic understanding of its general importance. In this issue of Molecular Ecology, Kirubakaran et al. () examine the role of recombination suppression in a particularly fascinating example of adaptation in the face of gene flow: the evolution of migratory differences between interbreeding populations of cod. Along the north coast of Norway, two types of cod breed in the near‐shore waters: a ‘stationary’ form that lives near the coast year round, and a ‘migratory’ form that lives far offshore and only returns to the coast to breed. Using a combination of approaches, Kirubakaran et al. () deftly demonstrate that the migratory form has completely fixed two adjacent inversions containing a suite of genes closely connected to migratory behaviour and feeding differences. This work provides an excellent example of how recombination suppression can facilitate adaptive divergence, and helps us understand the geographic and temporal scales over which genomic structural variation evolves.
Animals living in cooperative groups experience fundamentally different environments than their nonsocial relatives, potentially changing the strength of natural selection on some aspects of their ...behavior. Using a comparative approach, we examined a potential example of this phenomenon: an association between reduced levels of maternal care behavior and sociality in cobweb spiders. We compared 6 different measures of maternal care behavior between species from 2 independently derived social clades and subsocial species from sister clades. In natural nests, we measured the mean distance between egg sacs and the nearest female and the proportion of egg sacs being attended. In the lab, we measured a female's willingness to accept an egg sac, abandon her egg sac when disturbed, repair a damaged egg sac, and the speed at which a female reclaimed her egg sac when separated from it. Social species from both social clades scored significantly lower than subsocial species from sister clades on 6 and 4 of 6 of these assays of maternal care, respectively. We discuss alternative explanations of this pattern, including the potential role of relaxed natural selection in a social environment in permitting the evolution of a novel "low-parenting" phenotype.
Chromosomal inversions are often thought to facilitate local adaptation and population divergence because they can link multiple adaptive alleles into non‐recombining genomic blocks. Selection should ...thus be more efficient in driving inversion‐linked adaptive alleles to high frequency in a population, particularly in the face of maladaptive gene flow. But what if ecological conditions and hence selection on inversion‐linked alleles change? Reduced recombination within inversions could then constrain the formation of optimal combinations of pre‐existing alleles under these new ecological conditions. Here, we outline this idea of inversions limiting adaptation and divergence when ecological conditions change across time or space. We reason and use simulations to illustrate that the benefit of inversions for local adaptation and divergence under one set of ecological conditions can come with a concomitant constraint for adaptation to novel sets of ecological conditions. This limitation of inversions to adaptation may contribute to the maintenance of polymorphism within species.
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