Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?

Abstract

Human-mediated introductions are reshuffling species distribution on a global scale. Consequently, an increasing number of allopatric taxa are now brought into contact, promoting introgressive hybridization between incompletely isolated species and new adaptive gene transfer. The broadcast spawning marine species, Ciona robusta, has been recently introduced in the native range of its sister taxa, Ciona intestinalis, in the English Channel and North-East Atlantic. These sea squirts are highly divergent, yet hybridization has been reported by crossing experiments and genetic studies in the wild. Here, we examined the consequences of secondary contact between C. intestinalis and C. robusta in the English Channel. We produced genomes phased by transmission to infer the history of divergence and gene flow, and analyzed introgressed genomic tracts. Demographic inference revealed a history of secondary contact with a low overall rate of introgression. Introgressed tracts were short, segregating at low frequency, and scattered throughout the genome, suggesting traces of past contacts during the last 30 ky. However, we also uncovered a hotspot of introgression on chromosome 5, characterized by several hundred kb-long C. robusta haplotypes segregating in C. intestinalis, that introgressed during contemporary times the last 75 years. Although locally more frequent than the baseline level of introgression, C. robusta alleles are not fixed, even in the core region of the introgression hotspot. Still, linkage-disequilibrium patterns and haplotype-based tests suggest this genomic region is under recent positive selection. We further detected in the hotspot an over-representation of candidate SNPs lying on a cytochrome P450 gene with a high copy number of tandem repeats in the introgressed alleles. Cytochromes P450 are a superfamily of enzymes involved in detoxifying exogenous compounds, constituting a promising avenue for functional studies. These findings support that introgression of an adaptive allele is possible between very divergent genomes and that anthropogenic hybridization can provide the raw material for adaptation of native lineages in the Anthropocene.

Urban rendezvous along the seashore: Ports as Darwinian field labs for studying marine evolution in the Anthropocene

“…This recent introgression was previously missed even with the use of a large ancestry informative SNP panel, due to its very localized position in the genome (Bouchemousse et al, 2016; Le Moan et al, 2021). The analysis of whole‐genome sequences provided support that this introgression breakthrough is adaptive (Fraïsse et al, 2022).…”

A synthesis of biological invasion hypotheses associated with the introduction–naturalisation–invasion continuum

“…It can occur even at a late speciation stage, as recently documented by the introgression of the European native tunicate Ciona intestinalis by its introduced congener Ciona robusta , native to Asia, which have diverged 4 millions years ago and display synonymous divergence rate of 15% (Le Moan et al 2021). This latter case, which is presumably an adaptive introgression (Fraïsse et al 2022), is rare, as in most cases, introgression is expected to occur in the reverse direction, i.e. from the native to the introduced species Viard et al 2020).…”

Introgression between highly divergent sea squirt genomes: an adaptive breakthrough?

“…Supplementary Data is available from Zenodo (Fraïsse 2022a). Supplementary Figures, Tables and Scripts are available from Zenodo (Fraïsse 2022b).…”

“…Sequence reads have been deposited in NCBI Sequence Read Archive (SRA) under the accession number PRJNA813009. Supplementary Data is available from Zenodo (Fraïsse 2022a). Supplementary Figures, Tables and Scripts are available from Zenodo (Fraïsse 2022b).…”

“…Supplementary Data is available from Zenodo (Fraïsse 2022a). Supplementary Figures, Tables and Scripts are available from Zenodo (Fraïsse 2022b). Figure S8 Neighbor-joining trees of 50 Kb windows framing the "missing data region" (grey band) at the center of the chromosome 5 hotspot.…”