nominate Lesser Black-backed Gull (L. f. fuscus)

(last update: 10-11-2014 )

adult fuscus: April

Spring Baltic Gulls in Israel. Picture: Amir Ben Dov.

Phylogeography and colonization history of Lesser Black-backed Gulls (Larus fuscus) as revealed by mtDNA sequences

D. Liebers, A. J. Helbig, 2002 IN: Journal of Evolutionary Biology, Volume 15, Issue 6, pages 1021–1033, November 2002

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Abstract

Because of the differential amplitude of climatic oscillations, species living at northern latitudes are subject to more frequent and more severe range oscillations than species at southern latitudes. As a consequence, northern populations should, on average, be phylogenetically younger and possess less phylogeographical structure than closely related taxa further south. To test these predictions, we studied the mitochondrial-genetic population structure of NW Palearctic Lesser Black-backed Gulls (Larus fuscus group [= LBBG], five taxa) breeding at temperate to boreal latitudes from Iceland to the Taimyr Peninsula.
Results were compared with those previously obtained (Liebers et al. 2001. Mol. Ecol. 10: 2447) for more southerly breeding Yellow-legged Gulls (Larus cachinnans group, six taxa from the Atlantic Islands to Mongolia). Sequences of the hypervariable region I (HVR-I) of the mitochondrial control region revealed low within- and between-taxon sequence divergence, little genetic variation, a shallow haplotype phylogeny and poor phylogeographical structure in LBBGs compared with Yellow-legged Gulls.
Haplotype frequencies among the five northern taxa formed a stepped cline with significant gene flow restriction between the forms heuglini and fuscus, probably indicating a secondary contact with (partial?) reproductive isolation. Western forms of LBBG, among which mitochondrial gene flow appears unrestricted, show genetic signs of postglacial range expansion and population growth.
The Larus fuscus group is derived from a cachinnans-like ancestral population, probably in the Aralo-Caspian basin, and spread from east (NW Siberia) to west within the Palearctic.

Discussion

Differentiation of LBBG taxa

Our study of mitochondrial HVR-I sequences revealed that the five dark-mantled, NW Palearctic gull taxa collectively called LBBG are genetically very closely related. The extensive sharing of haplotypes among taxa (= incomplete lineage sorting) can be attributed to ongoing gene flow and ⁄ or very recent radiation (Avise, 2000). Although none of the five taxa was diagnosable using mitochondrial haplotypes, there were clear differences in haplotype frequencies between them. Indices of within-taxon genetic diversity showed that the eastern taxa (taimyrensis, heuglini) are genetically more diverse and have a longer population history than the western taxa. The latter, particularly graellsii, are very uniform genetically and show strong signs of recent population expansion. Thus the evidence indicates a westward expansion of LBBG populations from NW Siberia towards the NE Atlantic.
The genetic uniformity of graellsii is particularly interesting when contrasted with the population structure of Atlantic Yellow-legged Gulls (L. michahellis atlantis). Both inhabit adjacent and overlapping oceanic regions, but atlantis is genetically much more diverse with a high nucleotide diversity and low expansion coefficient (Liebers et al., 2001). Clearly, demographic histories of the two taxa must have been quite different. Atlantis is probably directly descended from a large ancestral population that did not experience severe bottlenecks or range restrictions during glaciations, because its marine range in the NE Atlantic was not strongly affected by advancing ice sheets.
Graellsii, on the other hand, is derived from a more easterly, fuscus-like ancestor that would have been subject to more severe population bottlenecking during glaciations and may have lost even more genetic variation during its relatively recent westward expansion.
The haplotype frequencies among LBBG taxa corresponded to a stepped cline (Barton, 1983) with the most pronounced 'step' between heuglini and fuscus. Estimated numbers of migrants were consistent with free gene flow between all graellsii and intermedius populations, but indicate a significant barrier to mitochondrial gene flow in the contact area between heuglini and fuscus along the southern White Sea. This is noteworthy, given that there are no ecological or topographical barriers between the ranges of the two taxa. Intrinsic factors such as different habitat preferences, timing of reproduction (Filchagov et al., 1992) or slight differences in mate recognition must be responsible for the maintenance of differentiation between them. Although breeding is locally sympatric (even on some of the same islands), neither mixed pairs nor birds with intermediate characters (potential hybrids) have been observed (Filchagov et al., 1992).

Population-genetic structure of northern vs. southern gulls

We documented profound differences in the mitochondrial-genetic population structure between northern LBBG and southern Yellow-legged Gulls, which is in good agreement with predictions derived from biogeographical theory (Dynesius & Jansson, 2000; Hewitt, 2000). Average sequence divergence, differentiation between taxa (FST) and the among-taxon component of molecular variance were all much lower in LBBG than in Yellow-legged Gulls. Estimates of the coalescence time of haplotypes found in LBBG are necessarily rough, not only because of the lack of a reliable rate calibration for the Charadriiform HVR-I, but also because of a large stochastic error associated with the small sequence divergence we found. The maximum divergence among LBBG haplotypes was 1.4% (six nucleotide differences among 430 sites, see Fig. 3). Assuming a rate of 8.48% change per 1 Mio years, the ancestral population of modern LBBG is estimated to have lived approximately 165 000 years ago. This contrasts with an equivalent age estimate of 490 000 years for nominate Larus cachinnans in the Aralo-Caspian basin (18 nucleotide differences, see Fig. 4 in Liebers et al., 2001). This revised estimate is older than the one we published previously, because we now used a better founded calibration rate (see 'Materials and Methods').

Lesser Black-backed Gulls were characterized by starlike haplotype phylogeny centred on two highly dominating haplotypes, while many rare haplotypes differed only by single substitutions. This pattern is typical of recent population expansion (Slatkin & Hudson, 1991; von Haeseler et al., 1996; Forster et al., 2001). In contrast, southern Yellow-legged Gulls showed a complex haplotype network with multiple, quite divergent clusters (Fig. 3) corresponding to long periods of multiregional differentiation. Northern gulls therefore are not only phylogenetically younger, but also less differentiated and less structured geographically than their closest relatives at more southerly latitudes. Presumably, range oscillations and associated variation in population size during Quaternary glacial cycles have affected LBBG much more than Yellow-legged Gulls, which enjoyed a larger and more stable long-term population size.
Similar patterns have been found in organisms as diverse as grasshoppers (Cooper et al., 1995), Nearctic and Palearctic fish species (Bernatchez & Wilson, 1998), European Crested Newts (Wallis & Arntzen, 1989) and North American woodrats (Hayes & Harrison, 1992), but few studies have addressed these questions in birds so far.
Atlantic Common Guillemot (Uria aalge), a widespread boreal seabird partly overlapping in range and ecologically comparable with Larus fuscus, also showed a star-like haplotype phylogeny and little sequence divergence, i.e. signs of recent population expansion (Moum & A´ rnason, 2001). Guillemots and Razorbills (Alca torda) displayed even less geographical partitioning of haplotype variation than LBBG, so their population-genetic architecture conformed to the pattern expected for species with strong range oscillations caused by glacial cycles. The same is true for those landbird species that have been adequately sampled, e.g. the Greenfinch Carduelis chloris (Merila¨ et al., 1997) and several passerine species in North America (overview: Zink, 1996). Most of these studies, with the notable exception of one on a Nearctic migratory warbler (Mila´ et al., 2000), did not compare phylogeographical structure of northern populations directly with that of conspecific (or closely related) southern populations ⁄ taxa. It is the direct contrast between closely related, ecologically equivalent forms at different latitudes, as we presented it here for gulls, that illustrates the differences in phylogeographical structure most prominently.

Taxonomic implications

It has been proposed recently (Sangster et al., 1998) to divide the NW-Palearctic dark-mantled gulls into three species: LBBG L. graellsii (incl. intermedius), Baltic Gull Larus fuscus, and Tundra Gull Larus heuglini (incl. taimyrensis). Can this suggestion be justified on the basis of a Biological Species Concept in the light of our mitochondrial-genetic results?
The split between heuglini and fuscus has received most support from phenotypic differentiation, perceived lack of interbreeding as well as behavioural and ecological segregation (breeding habitat, feeding behaviour) in the area of contact (Stegmann, 1934; Filchagov & Semashko, 1987; Filchagov et al., 1992; Rauste, 1999). The significant genetic differentiation we documented certainly indicates a reproductive barrier, although this may be incomplete. More sampling close to the contact zone would be needed to assess more precisely the extent to which gene flow is restricted. Extensive sharing of haplotypes between the two taxa may just reflect the recent separation from a common ancestor (ancestral polymorphism) rather than ongoing gene flow. Based on current evidence, fuscus and heuglini are best regarded as semispecies (intrinsic gene flow restriction, but probably not complete reproductive isolation).
Evidence for separating fuscus from intermedius⁄ graellsii is much weaker, both phenotypically and genetically. Notwithstanding the large gap between fuscus and intermedius sampling sites, the SW Finnish fuscus population was only marginally differentiated from intermedius in mtDNA. Further sampling in between would probably reveal a smooth cline in haplotype frequencies, compatible with the isolation-by-distance model. Based on phenotypic characters it is also not possible to draw a definite line between fuscus and intermedius (Jonsson, 1998), because characters vary within each taxon and differ only on

average (B (Barth, 1975; Bergmann, 1982; Cramp & Simmons, 1983; Strann & Vader, 1992). The most clear-cut differences are in moult and migration behaviour, characters that are evolutionarily highly flexible and under strong selection (cf. Helbig, 2002). In conclusion, there is so far no evidence for a significant reproductive barrier between fuscus and intermedius, they should thus be retained as members of the same species.

Last days of March or sometimes the first week of April: Larus fuscus circling in groups to migrate north to the breeding grounds.