Biology subjects

Connallon, T.

Publications and source records attributed to Connallon, T..

10 recordsLinked to original sources

bioRxiv2026

The evolution of context-specific dominance during selective sweeps

Dominance is a widespread feature of genetic variants which affects life-history traits and fitness. Although dominance is generally thought to be an intrinsic property of genetic variants, it can sometimes evolve, as in the classic case of melanism in the peppered moth. The broader question of how likely dominance is to evolve is, however, controversial, because conditions favouring dominance evolution are often restrictive. Here, we revisit Haldanes classic hypothesis that dominance might evolve during the spread of beneficial mutations to fixation (i.e., during selective sweeps). We first confirm results of earlier models that sweeps of unconditionally beneficial mutations generate little potential for dominance to evolve, even in cases where modifier alleles segregate prior to selective sweeps. However, when sweeping beneficial alleles trade off between different environments -- which we explore with the illustrative case of sexually antagonistic selection -- the scope for dominance evolution expands. This occurs because modifier alleles can alter dominance separately in each environment, increasing the mean fitness of heterozygotes, prolonging the sojourn time of the sweep, and generating more heterozygosity upon which the modifier can act. In extreme cases, beneficial mutations that were initially destined for fixation can undergo a "dominance reversal" as a result of dominance evolution, converting them to balanced polymorphisms. We quantify how regularly dominance reversals of sweeping sexually antagonistic alleles can be expected to evolve. Overall, our results highlight conditions that allow the dominance of beneficial mutations to evolve, which we discuss in light of data on the frequency of selective sweeps, standing genetic variation for modifiers, and plasticity of modifier effects.

evolutionary biology↗

bioRxiv2026

Characterising the detectable and invisible fractions of genomic loci under balancing selection

Balancing selection refers to scenarios where selection maintains genetic polymorphisms affecting fitness and its components. Empirical studies have documented specific cases of balancing selection, yet the general prevalence of balanced polymorphisms within genomes remains a topic of longstanding debate. Although genome-wide scans for signals of balancing selection suggest that it is rare, current methods are notoriously conservative and may identify only a small and unrepresentative fraction of loci evolving under balancing selection. What, then, are the proportions of loci under balancing selection that are detectable versus invisible to genome scans? Here, we address this question using a combination of analytical modelling and population genetic simulations. Our results provide quantitative support for the intuition that a large fraction of loci under balancing selection will be invisible to standard tests for balancing selection, with the detectable loci representing a biased subset with large and symmetrical fitness effects on different fitness components. Quantifying power across parameters that vary between species also shows that the detectable and invisible fractions of genomic loci under balancing selection are likely to differ substantially between organisms. For example, a Drosophila melanogaster-like ratio of mutation to recombination rates ([~]0.1) reduces detection power by roughly a quarter of the power expected with a human-like ratio ([~]1). This, combined with other evidence suggesting that balancing selection could be common in D. melanogaster, showcases how our appreciation of the prevalence of balancing selection is limited by our ability to detect its genomic signals, especially in those species where it might be common.

genetics↗

bioRxiv2025

Meta-analysis reveals the tempo of evolutionary parallelism of local adaptation between native and introduced ranges of plant species

Invasive species are valuable systems for evaluating evolutionary predictability, as populations in native and introduced ranges evolve separately, yet often encounter similar environmental challenges that select for parallel patterns of local adaptation across each range. However, it remains unclear how pervasive and strong such parallelism is and how rapidly it evolves. To address these questions, we first extended cline theory to predict evolutionary patterns of trait cline parallelism between ranges. We then carried out a meta-analysis of clinal divergence in native and introduced populations of the same plant species and evaluated the tempo of trait cline parallelism between ranges. We found that clines in introduced ranges were somewhat shallower than native range clines, and directions of clinal divergence were, on average, partially aligned between ranges, with extensive variation in parallelism among traits and species, including counter-clines between native and introduced ranges. The degree of evolutionary parallelism of clinal divergence strongly increased, and the prevalence of counter-clines decreased, with the time since introduction, where greater parallelism in older introductions was primarily caused by increased alignment in the direction of clinal divergence between ranges rather than changes in their relative magnitudes of divergence. We argue that these observations are consistent with a two-phased process of cline evolution across introduced ranges. In the first phase, misaligned clines between introduced and native ranges can arise during range expansions, often owing to demographic and genetic constraints that initially hinder the evolution of local adaptation within the new range. During the second phase, the evolution of local adaptation eventually resolves early instances of maladaptation across introduced ranges, leading to strong trait cline parallelism between native and introduced ranges.

evolutionary biology↗

bioRxiv2025

Dissecting contributions of directional and balancing selection to trajectories of mitochondrial haplotype evolution in Drosophila melanogaster.

Emerging evidence suggests mtDNA haplotypes contribute to fitness variation and local adaptation, with studies highlighting the potential for directional selection, imposed by distinct thermal environments, and negative frequency-dependent selection to shape spatial patterns of mtDNA haplotype diversity. However, the interplay between these different forms of selection remains unexplored. To address this, we conducted experimental evolution using Drosophila melanogaster populations derived from opposite ends of a latitudinal cline in Australia (Melbourne and Townsville), exposing them to contrasting thermal environments and varying starting frequencies of two mtDNA haplotypes (A1 and B1) that each segregate at high frequencies in natural populations. We paired this approach with population genetic simulations to estimate selection and its influence on haplotype evolutionary trajectories. We found that mtDNA haplotype frequencies were influenced by complex interactions among temperature, starting frequency, and nuclear genomic background (Melbourne, Townsville, or admixed). Simulations supported directional selection as a driver of haplotype frequencies in populations evolving at 17{degrees}C in the Melbourne background, and otherwise selection was predominantly balancing and shaped by negative frequency-dependent fitness effects of the haplotypes. Finally, our results suggest that the thermal environment is not the sole environmental variable shaping mitochondrial evolutionary dynamics and point to a possible role for mito-nuclear epistasis.

evolutionary biology↗

bioRxiv2025

A re-evaluation of Muller's sheltering hypothesis for the evolution of sex chromosome gene content

The first influential hypothesis for sex chromosome evolution was proposed in 1914 by H. J. Muller, who argued that once recombination was suppressed between the X and Y chromosomes, Y-linked genes become "sheltered" from selection, leading to accumulation of recessive loss-of-function (LOF) mutations and decay of Y-linked genes. The hypothesis fell out of favour in the 1970s because early mathematical models failed to support it and data on the dominance of lethal mutations were viewed as incompatible with the hypothesis. We reevaluate the main arguments against Mullers hypothesis and find that they do not conclusively exclude a role for sheltering in sex chromosome evolution. By relaxing restrictive assumptions of earlier models, we show that sheltering promotes fixation of LOF mutations with sexually dimorphic fitness effects, resulting in decay of X-linked genes that are exclusively expressed by males and Y-linked genes that are primarily, though not necessarily exclusively, expressed by females. We further show that drift and other processes contributing to Y degeneration (i.e., selective interference and regulatory evolution) expand conditions of Y-linked gene loss by sheltering. The actual contribution of sheltering to sex chromosome evolution hinges upon the distribution of dominance and sex-specific fitness effects of LOF mutations, which we discuss.

evolutionary biology↗

bioRxiv2025

A century of theories of balancing selection

Traits that affect organismal fitness are often very genetically variable. This genetic variation is vital for populations to adapt to their environments, but it is also surprising given that nature (after all) "selects" the best genotypes at the expense of those that fall short. Explaining the extensive genetic variation of fitness-related traits is thus a longstanding puzzle in evolutionary biology, with cascading implications for ecology, conservation, and human health. Balancing selection--an umbrella term for scenarios of natural selection that maintain genetic variation-- is a century-old explanation to resolve this paradox that has gained recent momentum from genome-scale methods for detecting it. Yet evaluating whether balancing selection can, in fact, resolve the paradox is challenging, given the logistical constraints of distinguishing balancing selection from alternative hypotheses and the daunting collection of theoretical models that formally underpin this debate. Here, we track the development of balancing selection theory over the last century and provide an accessible review of this rich collection of models. We first outline the range of biological scenarios that can generate balancing selection. We then examine how fundamental features of genetic systems--including non-random mating between individuals, differences in ploidy, genetic drift, and different genetic architectures of traits-- have been progressively incorporated into the theory. We end by linking these theoretical predictions to ongoing empirical efforts to understand the evolutionary processes that explain genetic variation.

evolutionary biology↗

bioRxiv2024

Copy number variation contributes to parallel local adaptation in an invasive plant

Adaptation is a critical determinant of the diversification, persistence, and geographic range limits of species. Yet the genetic basis of adaptation is often unknown and potentially underpinned by a wide range of mutational types - from single nucleotide changes to large-scale alterations of chromosome structure. Copy number variation (CNV) is thought to be an important source of adaptive genetic variation, as indicated by decades of candidate gene studies that point to CNVs underlying rapid adaptation to strong selective pressures. Nevertheless, population- genomic studies of CNVs face unique logistical challenges not encountered by other forms of genetic variation. Consequently, few studies have systematically investigated the contributions of CNVs to adaptation at a genome-wide scale. We present a genome-wide analysis of CNV contributing to the adaptation of an invasive weed, Ambrosia artemisiifolia - the first such study in an invasive pest. CNVs show clear signatures of parallel local adaptation between North American (native) and European (invaded) ranges, implying widespread reuse of CNVs during adaptation to shared heterogeneous patterns of selection. We used a local principal component analysis to genotype CNV regions in whole-genome sequences of samples collected over the last two centuries. We identified 16 large CNV regions of up to 11.85 megabases in length, six of which show signals of rapid evolutionary change, with pronounced frequency shifts between historic and modern populations. Our results provide compelling genome-wide evidence that copy number variation underlies rapid adaptation over contemporary timescales of natural populations. Significance StatementUsing a population-genomic approach, we identified copy number variants - stretches of DNA that can be either present, absent, or in multiple copies - displaying parallel signatures of local adaptation across the native and introduced ranges of the invasive weed Ambrosia artemisiifolia. We further identified 16 large copy number variants, some associated with ecologically important traits including sex allocation and height, that show strong signatures of selection over space, along with dramatic temporal changes over the past several decades. These results highlight the importance of an often-overlooked form of genomic variation in both local adaptation and rapid adaptation of invasive species.

evolutionary biology↗

bioRxiv2022

Large haploblocks underlie rapid adaptation in an invasive weed

Adaptation is the central feature and leading explanation for the evolutionary diversification of life. Adaptation is also notoriously difficult to study in nature, owing to its complexity and logistically prohibitive timescale. We leverage extensive contemporary and historical collections of Ambrosia artemisiifolia--an aggressively invasive weed and primary cause of pollen-induced hayfever--to track the phenotypic and genetic causes of recent local adaptation across its native and invasive ranges in North America and Europe, respectively. Large haploblocks-- indicative of chromosomal inversions--contain a disproportionate share (26%) of genomic regions conferring parallel adaptation to local climates between ranges, are associated with rapidly adapting traits, and exhibit dramatic frequency shifts over space and time. These results highlight the importance of large-effect standing variants in rapid adaptation, which have been critical to A. artemisiifolias global spread across vast climatic gradients.

evolutionary biology↗

bioRxiv2021

Polygenic signals of sexually antagonistic selection in contemporary human genomes

Sex differences in the fitness effects of genetic variants can influence the rate of adaptation and the maintenance of genetic variation. For example, "sexually antagonistic" (SA) variants, which are beneficial for one sex and harmful for the other, can both constrain adaptation and increase genetic variability for fitness components such as survival, fertility, and disease susceptibility. However, detecting variants with sex-differential fitness effects is difficult, requiring genome sequences and fitness measurements from large numbers of individuals. Here, we develop new theory for studying sex-differential selection across a complete life cycle, and test our models with genotypic and reproductive success data from ~250,000 UK Biobank individuals. We uncover polygenic signals of sex-differential selection affecting survival, reproductive success and overall fitness, with signals of sex-differential reproductive selection reflecting a combination of SA polymorphisms and sexually concordant polymorphisms in which the strength of selection differs between the sexes. Moreover, these signals hold up to rigorous controls that minimise the contributions of potential confounders, including sequence mapping errors, population structure, and ascertainment bias. Functional analyses reveal that sex-differentiated sites are enriched in phenotype-altering genomic regions, including coding regions and loci affecting a range of quantitative traits. Population genetic analyses show that sex-differentiated sites exhibit evolutionary histories dominated by genetic drift and/or transient balancing selection, but not long-term balancing selection, which is consistent with theoretical predictions of effectively weak SA balancing selection in historically small populations. Overall, our results are consistent with polygenic sex-differential--including SA--selection in humans. Evidence for sex-differential selection is particularly strong for variants affecting reproductive success, in which the potential contributions of non-random sampling to statistical signals of sex-differentiation can be excluded.

evolutionary biology↗

bioRxiv2020

The search for sexually antagonistic genes: Practical insights from studies of local adaptation and statistical genomics

Sexually antagonistic (SA) genetic variation--in which genotypes favoured in one sex are disfavoured in the other--is predicted to be common and has been documented in several animal and plant populations, yet we currently know little about its pervasiveness among species or its population genetic basis. Recent applications of genomics in studies of SA genetic variation have highlighted considerable methodological challenges to the identification and characterisation of SA genes, raising questions about the feasibility of genomic approaches for inferring SA selection. The related fields of local adaptation and statistical genomics have previously dealt with similar challenges, and lessons from these disciplines can therefore help overcome current difficulties in applying genomics to study SA genetic variation. Here, we integrate theoretical and analytical concepts from local adaptation and statistical genomics research--including FST and FIS statistics, genome-wide association studies (GWAS), pedigree analyses, reciprocal transplant studies, and evolve-and-resequence (E&R) experiments--to evaluate methods for identifying SA genes and genome-wide signals of SA genetic variation. We begin by developing theoretical models for between-sex FST and FIS, including explicit null distributions for each statistic, and using them to critically evaluate putative signals of sex-specific selection in previously published datasets. We then highlight new statistics that address some of the limitations of FST and FIS, along with applications of more direct approaches for characterising SA genetic variation, which incorporate explicit fitness measurements. We finish by presenting practical guidelines for the validation and evolutionary analysis of candidate SA genes and discussing promising empirical systems for future work. Impact SummaryGenome sequences carry a record of the evolutionary and demographic histories of natural populations. Research over the last two decades has dramatically improved our ability to detect genomic signals of adaptation by natural selection, including several widely-used methods for identifying genes underlying local adaptation and quantitative trait variation. Yet the application of these methods to identify sexually antagonistic (SA) genes--wherein variants that are adaptive for one sex are maladaptive for the other--remains under-explored, despite the potential importance of SA selection as a mechanism for maintaining genetic variation. Indeed, several lines of evidence suggest that SA genetic variation is common within animal and plant populations, underscoring the need for analytical methods that can reliably identify SA genes and genomic signals of SA genetic variation. Here, we integrate statistics and experimental designs that were originally developed within the fields of local adaptation and statistical genomics and apply them to the context of sex-specific adaptation and SA genetic variation. First, we evaluate and extend statistical methods for identifying signals of SA variation from genome sequence data alone. We then apply these methods to re-analyse previously published datasets on allele frequency differences between sexes--a putative signal of SA selection. Second, we highlight more direct approaches for identifying SA genetic variation, which utilise experimental evolution and statistical associations between individual genetic variants and fitness. Third, we provide guidelines for the biological validation, evolutionary analysis, and interpretation of candidate SA polymorphisms. By building upon the strong methodological foundations of local adaptation and statistical genomics research, we provide a roadmap for rigorous analyses of genetic data in the context of sex-specific adaptation, thereby facilitating insights into the role and pervasiveness of SA variation in adaptive evolution.

evolutionary biology↗