Gene-Flow in a Mosaic Hybrid Zone: Is Local Introgression Adaptive?

Abstract

Genome-wide scans of genetic differentiation between hybridizing taxa can identify genome regions with unusual rates of introgression. Regions of high differentiation might represent barriers to gene flow, while regions of low differentiation might indicate adaptive introgression-the spread of selectively beneficial alleles between reproductively isolated genetic backgrounds. Here we conduct a scan for unusual patterns of differentiation in a mosaic hybrid zone between two mussel species, Mytilus edulis and M. galloprovincialis. One outlying locus, mac-1, showed a characteristic footprint of local introgression, with abnormally high frequency of edulis-derived alleles in a patch of M. galloprovincialis enclosed within the mosaic zone, but low frequencies outside of the zone. Further analysis of DNA sequences showed that almost all of the edulis allelic diversity had introgressed into the M. galloprovincialis background in this patch. We then used a variety of approaches to test the hypothesis that there had been adaptive introgression at mac-1. Simulations and model fitting with maximum-likelihood and approximate Bayesian computation approaches suggested that adaptive introgression could generate a "soft sweep," which was qualitatively consistent with our data. Although the migration rate required was high, it was compatible with the functioning of an effective barrier to gene flow as revealed by demographic inferences. As such, adaptive introgression could explain both the reduced intraspecific differentiation around mac-1 and the high diversity of introgressed alleles, although a localized change in barrier strength may also be invoked. Together, our results emphasize the need to account for the complex history of secondary contacts in interpreting outlier loci. GENETIC barriers between related lineages are often semipermeable, varying in strength across the genome (Harrison 1986). As such, hybridization can lead to adaptive introgression, the transfer of selectively beneficial alleles between species (Parsons et al. 1993;Arnold 2004;Heliconius Genome Consortium 2012;Hedrick 2013). However, the frequency and importance of such hybridization events remain hotly debated (Mallet 2007;Abbott et al. 2013;Barton 2013). It is now common to address such questions by scanning genome sequences for regions of enhanced or reduced differentiation. Universally advantageous alleles can usually cross barriers to gene flow without much delay (e.g., Piálek and Barton 1997), and neutral loci linked to such alleles are expected to display unusually low levels of differentiation. In contrast, barrier loci will delay the introgression of neutral alleles in proportion to their linkage (Barton 1979;Barton and Bengtsson 1986); that is the basis for the investigation of genomic islands of differentiation (Turner et al. 2005;Hohenlohe et al. 2010;Nadeau et al. 2012).Interpreting regions of unusual differentiation can be difficult, not only because of variation in recombination across the genome (Nachman and Payseur 2012;Roesti ...

Marine stepping‐stones: Connectivity of Mytilus edulis populations between offshore energy installations

“…At all locations in the North Sea, hybridization between M. edulis and M. galloprovincialis was observed. This extends the known hybrid zone between these taxa further north than hitherto described (Bierne et al, ; Fraïsse et al, ). Possibly, as earlier studies were restricted to nearshore locations, artificial offshore hard substrates seem to house more mussel hybrids than nearshore substrates.…”

“…Mytilus edulis occurs naturally along shorelines of the northeast Atlantic from the high Arctic to the English Channel (Skibinski, Beardmore, & Cross, ). It hybridizes in stretched out mosaic hybrid zones with Mytilus trossulus , which inhabits the Baltic Sea in the east and with Mytilus galloprovincialis in the south (Fraïsse, Roux, Welch, & Bierne, ; Hilbish et al, ). Populations along the North Sea shores are M. edulis (Bierne et al, ; Luttikhuizen, Koolhaas, Bol, & Piersma, ) and therefore we expected the same for the offshore North Sea.…”

ABC inference of multi‐population divergence with admixture from unphased population genomic data

“…; Fraïsse et al . ). Although methods are available to incorporate this variation in models of divergence with gene flow (Sousa et al .…”

A framework for incorporating evolutionary genomics into biodiversity conservation and management

“…In the past, statistical evidence for determining the extent of hybridisation in nature has been difficult to obtain because patterns of genetic variation caused by hybridisation look similar to the patterns of genetic variation caused by the incomplete sorting of alleles that can accompany species divergence [212,214,215]. However, analytical approaches that use genome sequence data for robust inferences of hybridisation have recently been developed [215][216][217][218][219], which should help to better understand the extent and adaptive significance of hybridisation in nature.…”