bioRxiv Science⌕ Search

Biology subjects

Ebdon, S.

Publications and source records attributed to Ebdon, S..

10 recordsLinked to original sources

Stronger positive and purifying selection on X-linked genes in a species with paternal genome elimination

The faster-X effect predicts that X chromosomes may evolve more rapidly than autosomes due to selection on expressed recessive alleles. Quantifying the effect empirically usually requires numerous assumptions due to the impact of diplodiploid transmission dynamics, and so the relative contribution of dominance effects to sex chromosome evolution remains unclear. Springtails present a novel opportunity to ameliorate this. Male globular springtails have hemizygous X chromosomes, diploid autosomes, and eliminate their paternal genome during spermatogenesis. This leads to the autosomes matching the X chromosomes haplodiploid transmission. Hence, theoretically the X chromosomes and autosomes only differ in the fixation probability of male-beneficial alleles. We generated whole-genome resequencing and RNA-Seq data for the globular springtail Allacma fusca, to quantify the faster-X effect, leveraging this natural experiment. We find that after accounting for the deleterious distribution of fitness effects, and despite surprisingly depleted neutral X-linked diversity, the sex chromosomes show signals of both stronger purifying and positive selection, supporting the faster-X effect. Furthermore, we provide the first direct evidence for the loss of DNA methylation in Collembola. These results, obtained from a system where many of the confounding sex-autosome differences that typically obscure faster-X patterns are absent, support hemizygosity as a genuine driver of sex chromosome evolution and suggest that sex-linked genes could contribute disproportionately to adaptive potential.

evolutionary biology↗

338 coleopteran genomes reveal exceptional rearrangement variation compared to other insect orders

Chromosomal rearrangements reshape genome architecture, but rate variation across the tree of life remains poorly understood. Analysing 338 beetle (Coleoptera) genomes, we inferred eight ancestral linkage groups. No species retained these linkage groups, whereas the most frequent karyotypes of 10 or 11 chromosomes evolved at least 65 times through independent rearrangements. Rearrangement rates vary widely across lineages, with exceptionally high rates associated with major species radiations. Comparisons to 340 fly and 210 butterfly and moth genomes reveal the highest rates of long-term persistent rearrangements in beetles and that the beetle X chromosome traces back to the ancestor of Holometabola. We identified frequent X chromosome changes, mostly representing recent autosomal-X fusions, but no fissions. For autosomes, key rearrangement predictors include chromosome size, repeats and centromere position.

evolutionary biology↗

Hybrid breakdown is temporary and not expressed in a novel environment during 50 generations of experimental evolution in Tetranychus urticae hybrids

Hybridization, the interbreeding between species or genetically distinct populations, can lead to deleterious fitness consequences, but simultaneously it can boost adaptive potential by increasing genetic variation, especially in novel environments. However, how incompatibilities and beneficial genetic combinations interplay across generations remains poorly understood. Here, we tracked how two fitness proxies, the absolute number of adult offspring and the proportion of eggs that reached adulthood, evolve in parental and hybrid populations at three different time points over 50 generations, in both novel and ancestral environments. To test this, we used two geographically distinct populations with low divergence (Dxy=0.002) of the two-spotted spider mite (Tetranychus urticae). Across the first three generations, hybrids showed significantly lower fitness than parental populations in the ancestral environment, indicating incompatibilities between the parental genomes. In contrast, hybrid and parental fitnesses were similar in the novel environment, indicating that the impact of incompatibilities was minor compared to the selection imposed by the novel environment. However, after 50 generations, hybrids displayed similar fitness relative to parental populations in all environments, suggesting resolution of the incompatibilities. Furthermore, around generation 45, hybrids temporarily outperformed parental populations in a novel environment, suggesting a transient window of higher adaptive potential, before fitness stabilized again by generation 50. In conclusion, we show that hybrid populations of T. urticae can swiftly purge incompatibilities when genetic divergence is low. These findings suggest that the dynamics of incompatibility resolution and adaptive potential of novel haplotypes play out over a long time frame, highlighting the importance of tracking hybrid fitness past the first few generations.

evolutionary biology↗

340 dipteran genomes reveal the origin of Muller elements and sex chromosomes in Diptera

Diptera genome evolution is traditionally viewed through the lens of Drosophila melanogaster. To provide an unbiased picture of chromosome evolution in Diptera, we reconstructed six ancestral linkage groups (ALGs) and their rearrangements using 340 chromosome-level genome assemblies from 59 dipteran Families and two outgroups. Notably, Diptera ALGs are conserved in many Nematoceran lineages, while emergence of Brachycera coincided with four chromosomal fissions, which subsequently fused in various combinations. In Schizophora and relatives, a stable karyotype of five metacentric chromosomes and a chromosome homologous to the dot emerged that is remarkably stable with the notable exception of Drosophila, where the metacentric chromosomes became acrocentric Muller elements. Furthermore, our reconstruction reveals an ancient sex chromosome system associated with a small and gene-poor ALG that frequently fused to other chromosomes.

genomics↗

Rapid chromosomal evolution and oligocentromeric drive in sedges and rushes

The chromosomes of most eukaryotes have a single centromere, a specialised region involved in chromosome partitioning to daughter cells. Inter-chromosomal rearrangement risks generating chromosomes with two centromeres or none, disrupting segregation. Holocentric chromosomes, with centromere function distributed along the chromosome, are hypothesised to better tolerate inter-chromosomal rearrangement. However, evidence linking centromere organisation to rearrangement rate has been lacking. Sedges and rushes (Cyperaceae and Juncaceae) are specifically polycentric: they have several satellite-based centromeres per chromosome, whereas centromere location in "asatellitic" holocentrics is solely defined epigenetically. Using 36 chromosome-level genomes, we quantify extraordinary rearrangement rates and annotate candidate polycentromeres. Under our polycentromeric drive model, we expected satellite sequence, polycentromere architecture, and karyotype to evolve to exploit biased segregation during asymmetric meiosis. We find satellite turnover but also deep sequence conservation. Polycentromeric organisation seems constrained by chromosome size, and rearrangements are more stable when chromosomes have fewer polycentromeres, despite breakpoint regions being enriched for polycentromeres. Notably, we find putative monocentromeres in Carex myosuroides, which would be the first evidence for reversion to monocentricity in eukaryotes, and no identifiable polycentromeres in Cyperus rotundus, possibly a transition to asatellitic holocentricity. Overall, we demonstrate that this clade is powerful for linking centromere organisation to genome evolution.

genomics↗

Dynamic evolution of germ-line restricted chromosomes in three dark-winged fungus gnats (Sciaridae) revealed through chromosome level germline genomes.

Germline restricted chromosomes (GRCs) are an evolutionary mystery. While they seem to be important and perhaps indispensable in species they occur, they also show surprising variability in copy number and size. We are just beginning to understand the evolutionary significance of these chromosomes. One factor that impedes our understanding is that at present, few clades with these chromosomes have been studied in depth. We genomically investigate the GRCs in dark-winged fungus gnats (Sciaridae), a cosmopolitan and species-rich taxa which have harboured GRCs for at least 58 million years. Sciaridae species carry from 1-4 large GRCs which evolved through introgression from the Cecidomyiidae lineage. We produce the first male germline chromosome-scale genome assemblies for the sciarids Bradysia coprophila, B. impatiens, and Lycoriella ingenua. Comparing the GRCs both between and within species, we find that these chromosomes evolve in an extraordinarily dynamic fashion, with very little conservation of synteny or gene content. Puzzlingly, despite this variability, GRCs are gene rich and their genes are evolving under strong purifying selection. Additionally, we uncover evidence that somatic elimination of GRCs potentially occurs via a satellite mediated process. Our study sheds light on the mechanisms of meiosis, tissue restriction, chromosome elimination, and gives us a better appreciation for the diversity of genetic systems that not only persist, but thrive in nature. Significance statementGermline restricted chromosomes (GRCs) are a fascinating evolutionary puzzle. They are restricted to the germline early in development, have unusual transmission dynamics and are more variable than core chromosomes, but also seem to be indispensable in clades they occur in. We generate chromosome level GRC assemblies from three species of fungus gnats (Sciaridae, Diptera). We find that the GRCs, which originated via a cross-family hybridization event, are evolving much more dynamically than other chromosomes in the genome. The five GRCs we sequence are all large, gene-rich, and seem to carry functional genes, but contain mostly a non-overlapping gene set, suggesting that four of the five GRCs we sequenced did not evolve from the same original chromosome.

evolutionary biology↗

Genomic regions of current low hybridisation mark long-term barriers to gene flow in scarce swallowtail butterflies

Many closely related species continue to hybridise after millions of generations of divergence. However, the extent to which current patterning in hybrid zones connects back to the speciation process remains unclear: does evidence for current multilocus barriers support the hypothesis of speciation due to multilocus divergence? We analyse whole-genome sequencing data to investigate the speciation history of the scarce swallowtails Iphiclides podalirius and I. feisthamelii, which abut at a narrow ([~]25 km) contact zone north of the Pyrenees. We first quantify the heterogeneity of effective migration rate under a model of isolation with migration, using genomes sampled across the range to identify long-term barriers to gene flow. Secondly, we investigate the recent ancestry of individuals from the hybrid zone using genome polarisation and estimate the coupling coefficient under a model of a multilocus barrier. We infer a low rate of long-term gene flow from I. feisthamelii into I. podalirius the direction of which matches the admixture across the hybrid zone and complete reproductive isolation across{approx} 33% of the genome. Our contrast of recent and long-term gene flow shows that regions of low recent hybridisation are indeed enriched for long-term barriers which maintain divergence between these hybridising sister species. This paves the way for future analysis of the evolution of reproductive isolation along the speciation continuum. Author summaryEfforts to understand how new species evolve typically approach the problem through either: 1) investigating patterns of genetic exchange across hybrid zones -- where closely related species interbreed -- or 2) modelling the demographic history of closely related species. Both approaches are capable of quantifying variation in genetic exchange, or gene flow, along the genome to identify regions of reproductive isolation; yet they leverage genetic signatures across vastly different timescales. The former exploits very recent signatures, while the latter averages long-term signatures over the history of divergence. Hence, we can contrast the genomic distribution of barriers acting on these very different timescales to test how patterns of gene flow change across the speciation continuum. Here we use this strategy to capture the speciation dynamics of a pair of hybridising papilionid butterflies. Our results show that not only are these species continuing to produce hybrids after more than a million years since the onset of divergence, but there is a significant degree of concordance between patterns of gene flow observed along the genome across time scales.

evolutionary biology↗

The genome sequence of the scarce swallowtail, Iphiclides podalirius

The scarce swallowtail, Iphiclides podalirius (Linnaeus, 1758), is a species of butterfly in the family Papilionidae. Here we present a chromosome-level genome assembly for I. podalirius as well as gene and transposable element annotations. We estimate heterozygosity within different partitions of the genome and find a negative correlation between chromosome length and heterozygosity at fourfold-degenerate sites. This high quality genome assembly, the first for any species in the tribe Leptocircini, will be a valuable resource for population genomics in the genus Iphiclides and comparative genomics more generally.

evolutionary biology↗

Estimating the rates of crossover and gene conversion from individual genomes

Recombination can occur either as a result of crossover or gene conversion events. Population genetic methods for inferring the rate of recombination from patterns of linkage disequilibrium generally assume a simple model of recombination that only involves crossover events and ignore gene conversion. However, distinguishing the two processes is not only necessary for a complete description of recombination, but also essential for understanding the evolutionary consequences of inversions and other genomic partitions in which crossover (but not gene conversion) is reduced. We present heRho, a simple composite likelihood scheme for co-estimating the rate of crossover and gene conversion from individual diploid genomes. The method is based on analytic results for the distance-dependent probability of heterozygous and homozygous states at two loci. We apply heRho to simulations and data from the house mouse Mus musculus castaneus, a well studied model. Our analyses show i) that the rates of crossover and gene conversion can be accurately co-estimated at the level of individual chromosomes and ii) that previous estimates of the population scaled rate of recombination [Formula] under a pure crossover model are likely biased.

evolutionary biology↗

The Pleistocene species pump past its prime: evidence from European butterfly sister species

The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. Whilst it is clear that the contact zones that have been described for many sister taxa are secondary and have formed during the last interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the embryonic stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact-zone pairs. This suggests a possible role of selective sweeps affecting mitochondrial variation in maintaining contact zones. Impact SummaryThe influence of the Pleistocene glacial cycles on structuring species and genetic diversity in temperate taxa has permeated biogeographic and phylogeographic thinking for decades. Although phylogeographic studies have repeatedly claimed that the Pleistocene acted as a species pump, systematic tests of this idea based on robust estimates of species divergence are lacking. Here we estimate divergence times for all sister species pairs of European butterfly using genome-wide transcriptome data. We find that most species pairs are substantially older than the onset of Pleistocene glacial cycling. We also show that post divergence gene flow is restricted to pairs that form contact-zones. However, in contrast to expectations under a null model of allopatric speciation contract zone pairs are not necessarily younger than sympatric pairs.

evolutionary biology↗