Evolutionary history and seascape genomics of Harbour porpoises (Phocoena phocoena) across environmental gradients in the North Atlantic and adjacent waters

Abstract

The Harbour porpoise (Phocoena phocoena) is a highly mobile cetacean species which primarily occurs in coastal and shelf waters across the Northern hemisphere. It inhabits heterogeneous seascapes that vary broadly in salinity and temperature. Here we produced 74 whole genomes at intermediate coverage to study Harbour porpoise’s evolutionary history and investigate the role of local adaptation in the diversification into subspecies and populations. We identified ~6 million high quality SNPs sampled at 8 localities across the North Atlantic and adjacent waters, which we used for population structure, demographic, and genotype-environment association analyses. Our results support a genetic differentiation between three subspecies, and three distinct populations within the subspecies P.p. phocoena: Atlantic, Belt Sea and Proper Baltic Sea. Effective population size and Tajima’s D levels suggest a population contraction in both Black Sea and Iberian porpoises while a population expansion in the P.p. phocoena populations. Phylogenetic trees indicate a post-glacial colonization of Harbour porpoises from a southern refugium. Genotype-environment association analysis identified salinity as a major driver in genomic variation and we identified candidate genes putatively underlying adaptation to different salinity levels. Our study highlights the value of whole genome resequencing to unravel subtle population structure in highly mobile species and shows how strong environmental gradients and local adaptation may lead to population differentiation. The results have great conservation implications as we found major levels of inbreeding and low genetic diversity in the endangered Black Sea subspecies and identified the critically endangered Proper Baltic Sea porpoises as a separate population.

Genome-wide analysis of the harbour porpoise (Phocoena phocoena) indicates isolation-by-distance across the North Atlantic and local adaptation in adjacent waters

“…A further subdivision within the Baltic (BALT) region based on differences in genetics, morphology, and behavior has been repeatedly hypothesized, such that porpoises from BES and IBS would belong to two distinct populations (Celemin et al, 2023;Galatius et al, 2012;Lah et al, 2016;NAMMCO, 2019;Wiemann et al, 2010). This could be caused by a separation of these two groups during mating season and calving (Carlén et al, 2018;Huggenberger et al, 2002).…”

“…The porpoises across the North Atlantic show variation in diet (Aarefjord et al, 1995;Hammond et al, 2013;Víkingsson et al, 2003), differences in habitat use and activity patterns (Nuuttila et al, 2017), display ne scale morphological differences (Galatius et al, 2012;Härkönen et al, 2013;Viaud-Martínez et al, 2007) and exhibit signi cant isolation by distance (Lah et al, 2016). Based on these differences, local ecotypes have been postulated within the North Atlantic (Fontaine et al, 2017(Fontaine et al, , 2010Hammond et al, 2020;Olsen et al, 2022;Santos et al, 2004) and the Baltic Sea (Celemin et al, 2023;Galatius et al, 2012;Lah et al, 2016). The Baltic Sea was colonized from the North Sea during the end of the last glacial period (Sommer et al, 2008).…”

Genome-wide analysis of the harbour porpoise (Phocoena phocoena) indicates isolation-by-distance across the North Atlantic and potential local adaptation in adjacent waters

“…P. p. vomerina (North Pacific), unnamed (Pacific), P. p. meridionalis (South Atlantic Ocean and Iberian Sea), et al 2007) and significant isolation-by-distance (Lah et al 2016). Based on these differences, local ecotypes have been postulated within the North Atlantic (Fontaine et al 2010(Fontaine et al , 2017Hammond et al 2020;Olsen et al 2022;Santos et al 2004) and the Baltic Sea (Celemin et al 2023;Galatius et al 2012;Lah et al 2016). The Baltic Sea was colonized from the North Sea during the end of the last glacial period (Sommer et al 2008).…”

“…Today, the Baltic Sea differs in temperature and salinity from the North Sea/North Atlantic, as it has transitioned from freshwater to brackish and marine water since its formation in the Pleistocene (~ 15 kyr ago) (Paasche et al 2015;Varjopuro et al 2014). This could have promoted the divergence of harbour porpoises in the Baltic Sea from populations of the North Sea/North Atlantic (Celemin et al 2023;Lah et al 2016;Wiemann et al 2010).…”

“…Autenrieth et al 2018;Gao et al 2023;Neely et al 2018;Yu et al 2022;Yuan et al 2018;Zhou et al 2018). Due to the vastly improved resolution in comparison to studies on single loci, even subtle population differentiation can be detected (Cammen et al 2016;Çilingir et al 2022;de Greef et al 2022;Gallego-García et al 2021). In recent years genome wide single nucleotide polymorphisms (SNPs) have become valuable markers to identify population structure and boundaries (Çilingir et al 2022;Liu et al 2005;Morin et al 2009;Santure et al 2010).…”