Biology subjects

Kirkpatrick, M.

Publications and source records attributed to Kirkpatrick, M..

11 recordsLinked to original sources

bioRxiv2026

Recombination on 'non-recombining' sex chromosomes: empirical insights from the blackspotted stickleback

One hallmark of sex chromosome evolution is recombination suppression driven by inversions. The resulting non-recombining sex-linked regions accumulate deleterious mutations and functionally degenerate. The question therefore arises: why does selection not favor the reestablishment of recombination? Two (non-exclusive) explanations for this have been proposed: 1) selection to maintain linkage between the Primary Sex Determination Locus (PSDL) and sexually antagonistic loci - loci with alleles that are beneficial to one sex but detrimental to the other; and 2) the rarity of reversions - structural mutations that reverse the inversion that initially suppressed recombination. Empirical perspectives are sorely needed to evaluate the relevance of these models. Here, we characterised the intermediate stages of sex chromosome evolution in the blackspotted stickleback (Gasterosteus wheatlandi). We generated high-quality, phased assemblies and annotations for the X and Y chromosomes, as well as population-level sequencing. Using these data, we inferred distinct recombination loss events and their associated inversions. Most significantly, we find support from multiple lines of evidence for a [~]2 Mb recombination event that likely occurred via double crossover within an existing non-recombining inversion. This result highlights that rare recombination can occur within sex-linked inversions. Simulations suggest that such histories of gene flux may allow for a novel empirical framework, adapted from work on autosomal inversions, to infer evolutionary processes at work within sex-linked non-recombining regions and distinguish between models to explain the maintenance of recombination suppression on sex chromosomes. Significance StatementSex chromosomes have evolved countless times across eukaryotes and often lose the ability to recombine, causing them to degenerate over time. Why then, does recombination not restart to purge harmful mutations? By generating a high-quality genome assembly of the blackspotted stickleback, we discovered the strong empirical evidence of a sex chromosome undergoing a double-crossover event within a "non-recombining" region, which reset the degenerative process. This finding challenges the view that sex chromosome decay is a one-way street. Furthermore, using forward evolutionary simulations, we demonstrate that the genetic signatures left by such events could help identify the selective forces acting within non-recombining sex chromosomes, thereby explaining the maintenance of recombination suppression.

evolutionary biology↗

bioRxiv2025

The Acropora millepora microbiome is predicted by algal symbionts, host genetics, and environment

The coral microbiome is a critical component of coral health and resilience, yet it is unclear what factors drive coral microbiome composition, especially within the context of coral bleaching. Here, we use whole genome sequencing data combined with a machine learning approach (RDAforest) to assess predictors of the microbiome in 208 colonies of Acropora millepora from 12 reef sites in the Central Great Barrier Reef during a 2016 bleaching event. We characterized microbiome variation using k-mers. While some environmental variables, such as chlorophyll seasonal range and maximum degree heating weeks, were associated with microbiome composition, we find that host genetics and dominant photosymbionts were more powerful predictors. In contrast, bleaching score had negligible predictive power. The corals microbiome therefore correlates with dominant photosymbiont identity even during a bleaching event. The association of the microbiome with the environment suggests that the coral microbiome can serve as a proxy for environmental variation when environment cannot be measured directly, which may be especially useful in ancient DNA studies.

evolutionary biology↗

bioRxiv2024

Does Sex-Differential Gene Expression Drive Sex-Differential Selection in Humans?

Sex differences in human transcriptomes have been argued to drive sex-differential natural selection (SDS). Here, we show that previous evidence supporting this hypothesis has been largely unfounded. We develop a new method to test for a genome-wide relationship between sex differences in expression and selection on expression-influencing alleles (eQTLs). We apply it across 39 human tissues and find no evidence for a general relationship. We offer possible explanations for the lack of evidence, including that it is due in part to eQTL ascertainment bias towards sites under weak selection. We conclude that the drivers of ongoing SDS in humans remain to be identified.

evolutionary biology↗

bioRxiv2024

The battle of the sexes in humans is highly polygenic

Sex-differential selection (SDS), which occurs when the fitness effects of alleles differ between males and females, can have profound impacts on the maintenance of genetic variation, disease risk, and other key aspects of natural populations. Because the sexes mix their autosomal genomes each generation, quantifying SDS is not possible using conventional population genetic approaches. Here, we introduce a novel method that exploits subtle sex differences in haplotype frequencies resulting from SDS acting in the current generation. Using data from 300K individuals in the UK Biobank, we estimate the strength of SDS throughout the genome. While only a handful of loci under SDS are individually significant, we uncover polygenic signals of genome-wide SDS for both viability and fecundity. An interesting life-history tradeoff emerges: alleles that increase viability more in one sex increase fecundity more in the other sex. Lastly, we find evidence of SDS on fecundity acting on alleles affecting arm fat-free mass. Taken together, our findings connect the long-standing evidence of SDS acting on human phenotypes with its impact on the genome. Significance statementSelection often acts differently on females and males, as evidenced by the striking sexual dimorphism found in many taxa. As a result, alleles can have different fitness effects in each sex. Consequences can include higher levels of genetic variation and higher disease burdens in populations. This study introduces a novel method to quantify this sex-differential selection (SDS) and reveals that it acts throughout the human genome. We discovered a life history tradeoff between survival and fecundity in females and males and that SDS on fecundity acts on alleles affecting arm fat-free mass.

evolutionary biology↗

bioRxiv2024

Bacterial ecology and evolution converge on seasonal and decadal scales

Ecology and evolution are often viewed as distinct processes, which interact on contemporary time scales in microbiomes. To observe these processes in a natural system, we collected a two-decade, 471-sample freshwater lake time series, creating the longest metagenome dataset to date. Among 2,855 species-representative genomes, diverse species and strains followed cyclical seasonal patterns, and one in five species experienced decadal shifts in strain composition. The most globally abundant freshwater bacterium had constant species-level abundance, but environmental extremes appeared to trigger a shift in strain composition and positive selection of amino acid and nucleic acid metabolism genes. These genes identify organic nitrogen compounds as potential drivers of freshwater responses to global change. Seasonal and long-term strain dynamics could be regarded as ecological processes or equivalently as evolutionary change. Rather than as distinct processes that interact, we propose a conceptualization where ecology and evolution converge along a continuum to better describe change in diverse microbial communities.

evolutionary biology↗

bioRxiv2023

Mitonuclear sex determination? Empirical evidence frombivalves

Genetic elements encoded in nuclear DNA determine the sex of an individual in many animals. In bivalves, however, mitochondrial DNA (mtDNA) has been hypothesized to contribute to sex determination in lineages that possess doubly uniparental inheritance (DUI). In these cases, females transmit a female mtDNA (F mtDNA) to all offspring, while male mtDNA (M mtDNA) is transmitted only from fathers to sons. Because M mtDNA is inherited in the same way as Y chromosomes, it has been hypothesized that mtDNA may be responsible for sex determination. However, the role of mitochondrial and nuclear genes in sex determination has yet to be validated in DUI bivalves. In this study, we used DNA, RNA, and mitochondrial short non-coding RNA (sncRNA) sequencing to explore the role of mitochondrial and nuclear elements in the sexual development pathway of the freshwater mussel Potamilus streckersoni (Bivalvia: Unionida). We found that the M mtDNA shed a sncRNA partially within a male-specific mitochondrial gene that targeted pathways hypothesized to be involved in female development and mitophagy. RNA-seq confirmed the gene target was significantly upregulated in females, supporting a direct role of mitochondrial sncRNAs in gene silencing. These findings support the hypothesis that M mtDNA inhibits female development. Genome-wide patterns of genetic differentiation and heterozygosity did not support a nuclear sex determining region, although we cannot reject that nuclear factors are involved with sex determination. Our results provide further evidence that mitochondrial loci contribute to diverse, non-respiratory functions and provide a first glimpse into an unorthodox sex determining system.

evolutionary biology↗

bioRxiv2022

How many ecological niches are defined by the superabundant marine microbe Prochlorococcus?

Determining the identities, frequencies, and memberships of ecotypes in Prochlorococcus and other superabundant microbes (SAMs) is essential to studies of their evolution and ecology. This is challenging, however, because the extremely large population sizes of SAMs likely cause violations of foundational assumptions made by standard methods used in molecular evolution and phylogenetics. Here we present a tree-free likelihood method to identify ecotypes, which we define as populations with genome sequences whose high similarity is maintained by purifying selection. We applied the method to 96 genomes of the superabundant marine cyanobacterium Prochlorococcus and find that this sample is comprised of about 24 ecotypes, substantially more than the five major ecotypes that are generally recognized. The method presented here may prove useful with other superabundant microbes.

evolutionary biology↗

bioRxiv2022

A tale of two paths: The evolution of mitochondrial recombination in bivalves with doubly uniparental inheritance

In most animals, mitochondrial DNA is strictly maternally inherited and non-recombining. One exception to these assumptions is called doubly uniparental inheritance (DUI): a phenomenon involving the independent transmission of female and male mitochondrial genomes. DUI is known only from the molluscan class Bivalvia. The phylogenetic distribution of male mitochondrial DNA in bivalves is consistent with several evolutionary scenarios, including multiple independent gains, losses, and varying degrees of recombination with female mitochondrial DNA. In this study, we use phylogenetic methods to test male mitochondrial DNA origination hypotheses and infer the prevalence of mitochondrial recombination in bivalves with DUI. Phylogenetic modeling using site concordance factors supported a single origin of male mitochondrial DNA in bivalves coupled with recombination acting over long evolutionary timescales. Ongoing mitochondrial recombination is present in Mytilida and Venerida, which results in a pattern of concerted evolution of female and male mitochondrial DNA. Mitochondrial recombination could be favored to offset the deleterious effects of asexual inheritance and maintain mitonuclear compatibility across tissues. Cardiida and Unionida have gone without recent recombination, possibly due to an extension of the COX2 gene in male mitochondrial DNA. The loss of recombination may be neutral but could be connected to the role of M mtDNA in sex determination or sexual development. Our results support recombination events in DUI species may occur throughout their genomes. Future investigations may reveal more complex patterns of inheritance of recombinants, which could explain the retention of signal for a single origination of male mitochondrial DNA in protein coding genes.

evolutionary biology↗

bioRxiv2022

Amplification is the Primary Mode of Gene-by-Sex Interaction in Complex Human Traits

Sex differences in complex traits are suspected to be in part due to widespread gene-by-sex interactions (GxSex), but empirical evidence has been elusive. Here, we infer the mixture of ways polygenic effects on physiological traits covary between males and females. We find that GxSex is pervasive but acts primarily through systematic sex differences in the magnitude of many genetic effects ("amplification"), rather than in the identity of causal variants. Amplification patterns account for sex differences in trait variance. In some cases, testosterone may mediate amplification. Finally, we develop a population-genetic test linking GxSex to contemporary natural selection and find evidence for sexually antagonistic selection on variants affecting testosterone levels. Taken together, our results suggest that the amplification of polygenic effects is a common mode of GxSex that may contribute to sex differences and fuel their evolution. O_FIG O_LINKSMALLFIG WIDTH=200 HEIGHT=130 SRC="FIGDIR/small/490973v3_ufig1.gif" ALT="Figure 1"> View larger version (37K): org.highwire.dtl.DTLVardef@19c267eorg.highwire.dtl.DTLVardef@a32233org.highwire.dtl.DTLVardef@1a6daeorg.highwire.dtl.DTLVardef@116cbff_HPS_FORMAT_FIGEXP M_FIG C_FIG

genomics↗

bioRxiv2020

Evolution of the canonical sex chromosomes of the guppy and its relatives

The sex chromosomes of the guppy, Poecilia reticulata, and its close relatives are of particular interest: they are much younger than the highly degenerate sex chromosomes of model systems such as mammals and Drosophila melanogaster, and they carry many of the genes responsible for the males dramatic coloration. Over the last decade, several studies have analyzed these sex chromosomes using a variety of approaches including sequencing genomes and transcriptomes, cytology, and linkage mapping. Conflicting conclusions have emerged, in particular concerning the history of the sex chromosomes and the evolution of suppressed recombination between the X and Y. Here we address these controversies by reviewing the evidence and reanalyzing data. We find no support for a nonrecombining sex determining region (SDR) or evolutionary strata in P. reticulata. Further, we find that the evidence most strongly support the hypothesis that the SDRs of P. picta and P. wingei evolved independently after those lineages diverged. We identify possible causes of conflicting results in previous studies and suggest best practices going forward.

genomics↗

bioRxiv2020

Contrasting tempos of sex chromosome degeneration in sticklebacks

The steps of sex chromosome evolution are often thought to follow a predictable pattern and tempo, but few studies have examined how the outcomes of this process differ between closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and Japan Sea stickleback (G. nipponicus) have been well characterized. Little is known, however, about the sex chromosomes in their distantly related congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees of interspecific crosses to obtain the first phased X and Y genomic sequences from blackspotted sticklebacks. Using novel statistical methods, we demonstrate that the oldest stratum of the Gasterosteus sex chromosomes evolved on Chromosome 19 in the ancestor of all three species. Despite this shared ancestry, the sex chromosomes of the blackspotted stickleback have experienced much more extensive recombination suppression, XY differentiation, and Y degeneration than those of the other two species. The ancestral blackspotted stickleback Y chromosome fused with Chromosome 12 less than 1.4 million years ago, which may have been favored by the very small size of the recombining region on the ancestral sex chromosome. Recombination is also suppressed between the X and Y over the bulk of Chromosome 12, although it has experienced little degeneration. These results demonstrate that sex chromosome evolution does not always follow a predictable tempo.

evolutionary biology↗