Biology subjects

Martin, S. H.

Publications and source records attributed to Martin, S. H..

4 recordsLinked to original sources

bioRxiv2018

Sexually dimorphic gene expression and transcriptome evolution provides mixed evidence for a fast-Z effect in Heliconius

Sex chromosomes have different evolutionary properties as compared to the autosomes due to their hemizygous nature. In particular, recessive mutations are more readily exposed to selection, which can lead to faster rates of molecular evolution. Here, we report patterns of gene expression and molecular evolution in the sex chromosomes of a group of tropical butterflies. We first improved the completeness of the Heliconius melpomene reference annotation, a neotropical butterfly with a ZW sex determination system. Then we sequenced RNA from male and female whole abdomens and female ovary and gut tissue to identify sex and tissue specific gene expression profiles in H. melpomene. Using these expression profiles we compare sequence divergence and polymorphism, the strength of positive and negative selection and rates of adaptive evolution for Z and autosomal genes between two species of Heliconius butterflies, H. melpomene and H. erato.\n\nWe show that the rate of adaptive substitutions is higher for Z as compared to autosomal genes, but contrary to expectation it is also higher for male as compared to female biased genes. There is therefore mixed evidence that hemizygosity influences the rate of adaptive substitutions. Additionally, we find no significant increase in the rate of adaptive evolution or purifying selection on genes expressed in ovary tissue, a heterogametic specific tissue. Together our results provide limited support for fast-Z evolution. This contributes to a growing body of literature from other ZW systems that also provide mixed evidence for a fast-Z effect.

evolutionary biology↗

bioRxiv2018

Recombination rate variation shapes barriers to introgression across butterfly genomes

Hybridisation and introgression can dramatically alter the relationships among groups of species, leading to phylogenetic discordance across the genome and between populations. Introgression can also erode species differences over time, but selection against introgression at certain loci acts to maintain post-mating species barriers. Theory predicts that species barriers made up of many loci throughout the genome should lead to a broad correlation between introgression and recombination rate, which determines the extent to which selection on deleterious foreign alleles will affect neutral alleles at physically linked loci. Here we describe the variation in genealogical relationships across the genome among three species of Heliconius butterflies: H. melpomene, H. cydno and H. timareta, using whole genomes of 92 individuals, and ask whether this variation can be explained by heterogeneous barriers to introgression. We find that species relationships vary predictably at the chromosomal scale. By quantifying recombination rate and admixture proportions, we then show that rates of introgression are predicted by variation in recombination rate. This implies that species barriers are highly polygenic, with selection acting against introgressed alleles across most of the genome. In addition, long chromosomes, which have lower recombination rates, produce stronger barriers on average than short chromosomes. Finally, we find a consistent difference between two species pairs on either side of the Andes, which suggests differences in the architecture of the species barriers. Our findings illustrate how the combined effects of hybridisation, recombination and natural selection, acting at multitudes of loci over long periods, can dramatically sculpt the phylogenetic relationships among species.

evolutionary biology↗

bioRxiv2017

Patterns of Z chromosome divergence among Heliconius species highlight the importance of historical demography

Sex chromosomes are disproportionately involved in reproductive isolation and adaptation. In support of such a large-X effect, genome scans between recently diverged populations or species pairs often identify distinct patterns of divergence on the sex chromosome compared to autosomes. When measures of divergence between populations are higher on the sex chromosome compared to autosomes, such patterns could be interpreted as evidence for faster divergence on the sex chromosome, i.e. faster-X, or barriers to gene flow on the sex chromosome. However, demographic changes can strongly skew divergence estimates and are not always taken into consideration. We used 224 whole genome sequences representing 36 populations from two Heliconius butterfly clades (H. erato and H. melpomene) to explore patterns of Z chromosome divergence. We show that increased divergence compared to equilibrium expectations can in many cases be explained by demographic change. Among Heliconius erato populations, for instance, population size increase in the ancestral population can explain increased absolute divergence measures on the Z chromosome compared to the autosomes, as a result of increased ancestral Z chromosome genetic diversity. Nonetheless, we do identify increased divergence on the Z chromosome relative to the autosomes in parapatric or sympatric species comparisons that imply post-zygotic reproductive barriers. Using simulations, we show that this is consistent with reduced gene flow on the Z chromosome, perhaps due to greater accumulation of species incompatibilities. Our work demonstrates the importance of constructing an appropriate demographic null model in order to interpret patterns of divergence on the Z chromosome, but nonetheless provides evidence to support the Z chromosome as a strong barrier to gene flow in incipient Heliconius butterfly species.

evolutionary biology↗

bioRxiv2016

Recombination Suppression is Unlikely to Contribute to Speciation in Sympatric Heliconius Butterflies

Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of co-adapted gene combinations. The sympatric butterfly species H. melpomene and H. cydno are separated by many strong barriers, but the species still hybridise infrequently in the wild, with around 40% of the genome influenced by introgression. We tested the hypothesis that genetic barriers between the species are reinforced by inversions or other mechanisms to reduce between-species recombination rate. We constructed fine-scale recombination maps for Panamanian populations of both species and hybrids to directly measure recombination rate between these species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.\n\nAuthor SummaryIt is now possible to study the process of species formation by sequencing the genomes of multiple closely related species. Heliconius melpomene and Heliconius cydno are two butterfly species that have diverged over the past 2 million years and have different colour patterns, mate preferences and host plants. However, they still hybridise infrequently in the wild and exchange large parts of their genomes. Typically, when genomes are exchanged, chromosomes are recombined and gene combinations are broken up, preventing species from forming. Theory predicts that gene variants that define species might be linked together because of structural differences in their genomes, such as inverted pieces of chromosomes that will not be broken up when the species hybridise. However, in this paper, we use deep sequencing of large crosses of butterflies to show that there are no long chromosome regions that are not broken up during hybridisation, and no long chromosome inversions anywhere between the two genomes. This suggests that hybridisation is rare enough and mate preference is strong enough that inversions are not necessary to maintain the species barrier.

evolutionary biology↗