Genetic Differentiation at Nuclear and Mitochondrial Loci Among Large White-Headed Gulls: Sex-Biased Interspecific Gene Flow?

Crochet, Pierre‐André; Chen, Junjian Z.; Pons, Jean‐Marc; Lebreton, Jean‐Dominique; Hebert, Paul D. N.; Bonhomme, François

doi:10.1554/03-008

Cited by 39 publications

(69 citation statements)

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“…The amount of genetic variation within species (Table 4) is in line with previous estimates, partly based on the same samples (Crochet et al, 2003). Genetic differentiation between SMITHSONIANUS and MARINUS (Table 3) is high compared with other species of large white-headed group (compare with Sonsthagen et al, 2012), again consistent with previous estimates for the same species (Crochet et al, 2003).…”

Section: Microsatellitessupporting

confidence: 90%

“…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).…”

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confidence: 99%

“…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).…”

mentioning

confidence: 99%

“…These species include some of the best documented avian hybrid zones (Hoffman et al, 1978;Bell, 1997;Good et al, 2000;Good, 2002;Gay et al, 2007Gay et al, , 2009Neubauer et al, 2009), and are remarkable for their low level of interspecific genetic differentiation compared with most biological species of birds, resulting from recent speciation events and on-going interspecific gene flow Crochet et al, 2003; Vigfú sdó ttir et al, 2008;Sternkopf et al, 2010;Sonsthagen et al, 2012). 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.…”

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confidence: 99%

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

et al. 2013

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Recent genetic studies have shown that introgression rates among loci may greatly vary according to their location in the genome. In particular, several cases of mito-nuclear discordances have been reported for a wide range of organisms. In the present study, we examine the causes of discordance between mitochondrial (mtDNA) and nuclear DNA introgression detected in North American populations of the Great Black-backed Gull (Larus marinus), a Holarctic species, from the Nearctic North American Herring Gull (Larus smithsonianus). Our results show that extensive unidirectional mtDNA introgression from Larus smithsonianus into Larus marinus in North America cannot be explained by ancestral polymorphism but most likely results from ancient hybridization events occurring when Larus marinus invaded the North America. Conversely, our nuclear DNA results based on 12 microsatellites detected very little introgression from Larus smithsonianus into North American Larus marinus. We discuss these results in the framework of demographic and selective mechanisms that have been postulated to explain mitonuclear discrepancies. We were unable to demonstrate selection as the main cause of mito-nuclear introgression discordance but cannot dismiss the possible role of selection in the observed pattern. Among demographic explanations, only drift in small populations and bias in mate choice in an invasive context may explain our results. As it is often difficult to demonstrate that selection may be the main factor driving the introgression of mitochondrial DNA in natural populations, we advocate that evaluating alternative demographic neutral hypotheses may help to indirectly support or reject hypotheses invoking selective processes. Heredity (2014) 112, 226-239; doi:10.1038/hdy.2013; published online 9 October 2013 Keywords: hybridization; mitochondrial DNA; microsatellites; speciation; Larus; North America INTRODUCTION Recent genetic studies have shown that at least 25% of plant species and 10% of animal species are involved in natural hybridization and potential introgression (Mallet, 2005). In birds, around 10% of species are known to hybridize (Grant and Grant, 1992), with some families having a strong propensity for hybridization. In Paradisaeidae (birds of paradise), for example, 43% of species hybridize in nature (Mallet, 2005). How these species can maintain their behavioral, phenotypic and ecological differences in the face of prevailing interspecific gene flow is an exciting question for speciation studies (for example, Pinho and Hey, 2010;Rice et al., 2011). Relevant information regarding the consequences of interspecific gene flow on a species' genome can be gained from examining variations in the pattern of introgression among loci (for example, Barton and Hewitt, 1985;Barton and Gale, 1993;Gay et al., 2007;Luttikhuizen et al., 2012). Indeed, one general pattern that emerges from recent studies is that introgression rates among loci may greatly vary according to their location in the genome. In particular, several studies...

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Section: Microsatellitessupporting

confidence: 90%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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

et al. 2013

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“…Sub-populations in a metapopulation with such selective, uneven gene flow could enjoy a relative independence for the benefit of local adaptation and, at the same time, share advantageous mutations through limited gene flow. This notion is in agreement with the high genetic similarity between many distinct species that are not separated by strong physical barriers, such as those observed in Drosophila (Ranz et al, 2003), birds (Crochet et al, 2003;Lijtmaer et al, 2003) and Lepidoptera (Presgraves, 2002). Given the prevalence of Haldane's rule, sex-biased genetic incompatibilities could be a major driving force behind such genomic divergence.…”

Section: Discussionsupporting

confidence: 80%

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

2007

Heredity

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In animals, hybrid sterility and inviability between closely related species often affect only the heterogametic sex (XY). This widespread phenomenon, known as Haldane's rule, is an early speciation event found across broad taxa, but the role of heterogametic hybrid incompatibilities, as opposed to homogametic ones, as a barrier in a speciation process remains obscure. It has been hypothesized that heterogametic incompatibility may be a more efficient mechanism in driving speciation. The population dynamics after (rather than before) the occurrence of sex-biased incompatibilities may account for Haldane's rule. In this study, a recursion model of hybrid zones was developed to investigate the differences between heterogametic and homogametic incompatibilities. The selection strengths and selection patterns of sex chromosome-linked, two-locus BatesonDobzhansky-Muller (BDM) genetic incompatibilities were examined. It is noted that a sex-biased hybrid incompatibility in a hybrid zone confers asymmetric and uneven impedance to gene flow. The clines of different loci in such a hybrid zone displayed diverse differentiation in their width, steepness and asymmetry. Alleles involved in the incompatibility face much stronger resistance to cross a hybrid zone. Different sexbiased BDM incompatibilities also affect the flow of neutral alleles differently. Compared to a homogametic one, heterogametic incompatibility is a weaker but more asymmetric barrier. These unique patterns of gene flow may explain uneven divergence among different genomic regions during speciation between some closely related species.

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Hybridization among Arctic white‐headed gulls (Larus spp.) obscures the genetic legacy of the Pleistocene

Sonsthagen

Chesser

Bell

et al. 2012

Ecology and Evolution

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We studied the influence of glacial oscillations on the genetic structure of seven species of white-headed gull that breed at high latitudes (Larus argentatus, L. canus, L. glaucescens, L. glaucoides, L. hyperboreus, L. schistisagus, and L. thayeri). We evaluated localities hypothesized as ice-free areas or glacial refugia in other Arctic vertebrates using molecular data from 11 microsatellite loci, mitochondrial DNA (mtDNA) control region, and six nuclear introns for 32 populations across the Holarctic. Moderate levels of genetic structure were observed for microsatellites (FST= 0.129), introns (ΦST= 0.185), and mtDNA control region (ΦST= 0.461), with among-group variation maximized when populations were grouped based on subspecific classification. Two haplotype and at least two allele groups were observed across all loci. However, no haplotype/allele group was composed solely of individuals of a single species, a pattern consistent with recent divergence. Furthermore, northernmost populations were not well differentiated and among-group variation was maximized when L. argentatus and L. hyberboreus populations were grouped by locality rather than species, indicating recent hybridization. Four populations are located in putative Pleistocene glacial refugia and had larger τ estimates than the other 28 populations. However, we were unable to substantiate these putative refugia using coalescent theory, as all populations had genetic signatures of stability based on mtDNA. The extent of haplotype and allele sharing among Arctic white-headed gull species is noteworthy. Studies of other Arctic taxa have generally revealed species-specific clusters as well as genetic structure within species, usually correlated with geography. Aspects of white-headed gull behavioral biology, such as colonization ability and propensity to hybridize, as well as their recent evolutionary history, have likely played a large role in the limited genetic structure observed.

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Genetic Differentiation at Nuclear and Mitochondrial Loci Among Large White-Headed Gulls: Sex-Biased Interspecific Gene Flow?

Cited by 39 publications

References 45 publications

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

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

Differential barrier strength and allele frequencies in hybrid zones maintained by sex-biased hybrid incompatibilities

Hybridization among Arctic white‐headed gulls (Larus spp.) obscures the genetic legacy of the Pleistocene

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