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

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. Author summary Introgression, the transfer of genetic material by hybridization between taxa, is increasingly recognized to sometimes persist for long periods during species divergence. However, the evolutionary consequences of human-induced introgression remain largely unknown, especially in the marine realm. While some argue it poses a threat to the genome integrity of native species, others consider it has a great potential to fuel adaptation. In this work, we quantify the magnitude and genomic distribution of introgression after secondary contact between a native sea squirt and its divergently related sister species recently introduced in the English Channel. The genome-wide pattern suggests introgression is mostly impeded between these two incompatible genomes. We nonetheless found a hotspot of long tracts that recently introgressed in a single region of the genome, with a clear footprint of recent positive selection. In the center of the hotspot, we further detected a promising candidate gene for adaptive introgression: a cytochrome P450 detoxifying enzyme with a high copy number in the introgressed allele. Therefore, our results support that adaptive introgression can remain possible between very divergent genomes and that anthropogenic hybridization can provide the raw material for the adaptation of native lineages in the Anthropocene.