The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic–Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels

Abstract

The hidden side of a major marine biogeographic boundary: a wide mosaic hybrid zone at the Atlantic-Mediterranean divide reveals the complex interaction between natural and genetic barriers in mussels. AbstractThe Almeria-Oran Front (AOF) is a recognised hotspot of genetic differentiation in the sea, with genetic discontinuities reported in more than 50 species. The AOF is a barrier to dispersal and an ecological boundary, and both facts can explain the position of these genetic breaks. However, the maintenance of genetic differentiation is likely reinforced by genetic barriers. A general drawback of previous studies is an insufficient density of sampling sites at the transition zone with a conspicuous lack of samples from the southern coastline. We analysed the fine-scale genetic structure in the mussel Mytilus galloprovincialis with a few ancestry-informative loci previously identified from genome scans. We discovered a 600 km wide mosaic hybrid zone eastward of the AOF along the Algerian coasts. This mosaic zone provides a new twist to our understanding of the Atlantic-Mediterranean transition because it demonstrates the two lineages can live in sympatry with ample opportunities to interbreed in a large area, but hardly do. This implies some form of reproductive isolation must exist to maintain the two genetic backgrounds locally cohesive. The mosaic zone ends with an abrupt genetic shift at a barrier to dispersal in the Gulf of Bejaia, Eastern Algeria.Simulations of endogenous or exogenous selection in models that account for the geography and hydrodynamic features of the region support the hypothesis that sister hybrid zones could have been differentially trapped at two alternative barriers to dispersal and/or environmental boundaries, at Almeria in the north and Bejaia in the south. A preponderantly unidirectional north-south gene flow next to the AOF can also maintain a patch of an intrinsically maintained genetic background in the south and the mosaic structure, even in the absence of local adaptation. Our results concur with the coupling hypothesis that suggests natural barriers mostly explain the position of genetic breaks while their maintenance must additionally require genetic barriers.

Massive gene presence/absence variation in the mussel genome as an adaptive strategy: first evidence of a pan-genome in Metazoa

“…The Mytilus genus has a complex evolutionary history, characterized by extensive gene flow among congeneric species, a process which is still ongoing in mosaic hybrid zones (42)(43)(44). However, the analysis of nuclear and mitochondrial genetic markers ruled out the possibility that our resequenced individuals were hybrids between M. galloprovincialis and other Mytilus species (Supplementary Data Note 7), which suggest that dispensable genes are unlikely to be recently introgressed allelic variants that cannot be mapped to the reference genome due to their sequence divergence (Supplementary Data Note 9).…”

“…Although intrinsic postzygotic selection has been invoked as one of the most likely mechanisms underpinning the preservation of mosaic hybrid zones (44,48), the nature of this process still remains to be elucidated. Here we postulate that the reduced fertility of the offspring produced by individuals carrying "structurally incompatible" chromosomes may be key for explaining post-zygotic selection and the maintenance of the pan-genome architecture in mussels.…”

Twin introductions by independent invader mussel lineages are both associated with recent admixture with a native congener in Australia

“…In the absence of complete reproductive barriers, introgression may promote successful introductions through the spread of locally favoured variants into introduced genomic backgrounds (Hovick & Whitney, 2014;Schierenbeck & Ellstrand, 2009). Hybridization may also impede invasions by trapping species barriers at environmental boundaries (Bierne, Welch, Loire, Bonhomme, & David, 2011;El Ayari, Menif, Hamer, Cahill, & Bierne, 2019;Kovach et al, 2016).…”

How do species barriers decay? Concordance and local introgression in mosaic hybrid zones of mussels

“…In Scotland, no local M. edulis were sampled, but the central population exhibits variable hybrid indexes, and so resembles Brittany more than Aquitaine. The Algerian hybrid zone was sampled most extensively (El Ayari et al, 2019). As previously shown with 4 markers (El Ayari et al, 2019), the distribution of hybrid indexes is wide, and the zone extends to around 600 km.…”

“…This is well illustrated in the complex of marine mussels, comprising the three species M. trossulus, M. edulis and M. galloprovincialis. This Mytilus species complex is subdivided into a mosaic of semi-isolated genetic clusters, by numerous hybrid zones El Ayari, Trigui El Menif, Hamer, Cahill, & Bierne, 2019;Fraïsse, Belkhir, et al, 2016;Riginos & Cunningham, 2005;Strelkov, Katolikova, & Väinolä, 2017). In the northern hemisphere all three species form a geographic mosaic delimited by multiple hybrid zones (Fraïsse, Belkhir, et al, 2016).…”