Introgressive hybridization and the evolutionary history of the herring gull complex revealed by mitochondrial and nuclear DNA

Abstract

BackgroundBased on extensive mitochondrial DNA (mtDNA) sequence data, we previously showed that the model of speciation among species of herring gull (Larus argentatus) complex was not that of a ring species, but most likely due more complex speciation scenario's. We also found that two species, herring gull and glaucous gull (L. hyperboreus) displayed an unexpected biphyletic distribution of their mtDNA haplotypes. It was evident that mtDNA sequence data alone were far from sufficient to obtain a more accurate and detailed insight into the demographic processes that underlie speciation of this complex, and that extensive autosomal genetic analysis was warranted.ResultsFor this reason, the present study focuses on the reconstruction of the phylogeographic history of a limited number of gull species by means of a combined approach of mtDNA sequence data and 230 autosomal amplified fragment length polymorphism (AFLP) loci. At the species level, the mtDNA and AFLP genetic data were largely congruent. Not only for argentatus and hyperboreus, but also among a third species, great black-backed gull (L. marinus) we observed two distinct groups of mtDNA sequence haplotypes. Based on the AFLP data we were also able to detect distinct genetic subgroups among the various argentatus, hyperboreus, and marinus populations, supporting our initial hypothesis that complex demographic scenario's underlie speciation in the herring gull complex.ConclusionsWe present evidence that for each of these three biphyletic gull species, extensive mtDNA introgression could have taken place among the various geographically distinct subpopulations, or even among current species. Moreover, based on a large number of autosomal AFLP loci, we found evidence for distinct and complex demographic scenario's for each of the three species we studied. A more refined insight into the exact phylogeographic history within the herring gull complex is still impossible, and requires detailed autosomal sequence information, a topic of our future studies.

Extensive mitochondrial introgression in North American Great Black-backed Gulls (Larus marinus) from the American Herring Gull (Larus smithsonianus) with little nuclear DNA impact

“…In accordance with the results from Sternkopf et al (2010), we detected an extensive introgression of mtDNA from SMITHSONIANUS into North American MARINUS. The discrepancy between our observed frequency of SMITHSONIANUS haplotypes into MARINUS (57%) and the frequency (34%) of the study from Sternkopf et al (2010) might result from a simple sampling variance, but it is also possible that there is a geographical variation in SMITHSONIANUS haplotype frequency in MAR-INUS, with north-westernmost populations harbouring fewer of the introgressed haplotypes. When combining samples from both studies, 37 MARINUS specimens from North America out of the 79 (hence 47%) carry mitochondria inherited from SMITHSONIANUS parentage.…”

“…Extensive introgression of mtDNA has been documented in several species (Crochet et al, 2003;Gay et al, 2007;Sternkopf et al, 2010;Sonsthagen et al, 2012). They thus constitute a promising model to address the causes of discordance between mtDNA and nuclear DNA introgression and the consequences of interspecific hybridization on the outcome of speciation processes.Extensive mtDNA introgression has been documented between Great Black-backed Gull (Larus marinus) and American Herring Gull (Larus smithsonianus) in North America (Crochet et al, 2003;Sternkopf et al, 2010). Great Black-backed Gull (MARINUS hereafter) is a Holarctic species distributed in Western Europe, Greenland and eastern North America (Olsen and Larsson, 2004) and is a member of a clade comprising several western European gull species closely related to the Herring Gull (Crochet et al, 2003;Liebers et al, 2004;Sternkopf et al, 2010).…”

“…Genetic data suggest that MARINUS originated in Europe and colonized eastern North American coast where it came into secondary contact with SMITHSO-NIANUS (Crochet et al, 2003;Sternkopf et al, 2010). Currently, a large proportion of North American MARINUS carries SMITHSONIANUS mtDNA haplotypes (the SMI haplotype hereafter) (Sternkopf et al, 2010). As only American MARINUS share SMI mtDNA haplotypes with SMITHSO-NIANUS, whereas SMI haplotypes are completely absent from Europe (even in other species of the Herring Gull complex), MARINUS populations in North America likely received SMI haplotypes by introgression rather than through the persistence of ancestral polymorphism in both species.…”

“…Second, lineage sharing only occurs in North America where they are sympatric and never in Europe where L. smithsonianus does not occur. As the shared HVR-I and cyt b haplotypes are observed at high frequency in these two species (Crochet et al, 2003, Sternkopf et al, 2010, it is unlikely that the North American MARINUS population was introgressed by gull species other than L. smithsonianus.Phenotypic (such as large size) and behavioural (foraging and breeding) differences distinguish L. marinus from other members of the Herring Gull complex (Burger and Gochfeld, 1996). Due to these phenotypic and behavioural differences, L. marinus is considered relatively reproductively isolated from co-occurring gull species (Liebers et al, 2004).…”

Hybridization and genetic introgression in birds

“…genetic homogenization 1b fusion of species de-speciation reverse speciation, speciation in reverse Seehausen et al 1997Seehausen et al , 2008Seehausen 2006;Taylor et al 2006 Geospiza Grant & Grant 1997, 2008a, 2008bGrant et al 2003, 2004Grant & Grant 2002, 2006Grant et al 2003Grant & Grant 2008aSaetre & Saether 2010Grant & Grant 2008aDabrowski et al 2005Neubauer et al 2009;Sternkopf et al 2010 Aquila clange A. pomarina 16 Vali et al 2010a 1500km 10 100 Rhymer et al 1994;Allendorf et al 2001;Peteres et al 2007 Anas …”