Search tips
Search criteria 


Logo of procbThe Royal Society PublishingProceedings BAboutBrowse by SubjectAlertsFree Trial
Proc Biol Sci. 2004 May 7; 271(1542): 893–901.
PMCID: PMC1691675

The herring gull complex is not a ring species.


Under what circumstances speciation in sexually reproducing animals can occur without geographical disjunction is still controversial. According to the ring-species model, a reproductive barrier may arise through 'isolation by distance' when peripheral populations of a species meet after expanding around some uninhabitable barrier. The classical example of this kind of speciation is the herring gull (Larus argentatus) complex, with a circumpolar distribution in the Northern Hemisphere. Based on mitochondrial DNA variation among 21 gull taxa, we show that members of this complex differentiated largely in allopatry following multiple vicariance and long-distance-colonization events, not primarily through isolation by distance. Reproductive isolation evolved more rapidly between some lineages than between others, irrespective of their genetic distance. Extant taxa are the result of divergent as well as reticulate evolution between two ancestral lineages originally separated in a North Atlantic refugium and a continental Eurasian refugium, respectively. Continental birds expanded along the entire north Eurasian coast and via Beringia into North America. Contrary to the ring-species model, we find no genetic evidence for a closure of the circumpolar ring through colonization of Europe by North American herring gulls. However, closure of the ring in the opposite direction may be imminent, with lesser black-backed gulls about to colonize North America.

Full Text

The Full Text of this article is available as a PDF (918K).

Supplementary Material

Supplementary data file:

Selected References

These references are in PubMed. This may not be the complete list of references from this article.
  • Bandelt HJ, Forster P, Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol. 1999 Jan;16(1):37–48. [PubMed]
  • de Knijff P, Denkers F, van Swelm ND, Kuiper M. Genetic affinities within the herring gull Larus argentatus assemblage revealed by AFLP genotyping. J Mol Evol. 2001 Jan;52(1):85–93. [PubMed]
  • Desjardins P, Morais R. Sequence and gene organization of the chicken mitochondrial genome. A novel gene order in higher vertebrates. J Mol Biol. 1990 Apr 20;212(4):599–634. [PubMed]
  • Excoffier L, Smouse PE, Quattro JM. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 1992 Jun;131(2):479–491. [PubMed]
  • Fleischer RC, McIntosh CE, Tarr CL. Evolution on a volcanic conveyor belt: using phylogeographic reconstructions and K-Ar-based ages of the Hawaiian Islands to estimate molecular evolutionary rates. Mol Ecol. 1998 Apr;7(4):533–545. [PubMed]
  • Gaggiotti OE, Excoffier L. A simple method of removing the effect of a bottleneck and unequal population sizes on pairwise genetic distances. Proc Biol Sci. 2000 Jan 7;267(1438):81–87. [PMC free article] [PubMed]
  • Grant PR, Grant BR. Genetics and the origin of bird species. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7768–7775. [PubMed]
  • Huelsenbeck JP, Ronquist F, Nielsen R, Bollback JP. Bayesian inference of phylogeny and its impact on evolutionary biology. Science. 2001 Dec 14;294(5550):2310–2314. [PubMed]
  • Irwin DE, Irwin JH, Price TD. Ring species as bridges between microevolution and speciation. Genetica. 2001;112-113:223–243. [PubMed]
  • Irwin DE, Bensch S, Price TD. Speciation in a ring. Nature. 2001 Jan 18;409(6818):333–337. [PubMed]
  • Kvist Laura, Martens Jochen, Higuchi Hiroyoshi, Nazarenko Alexander A, Valchuk Olga P, Orell Markku. Evolution and genetic structure of the great tit (Parus major) complex. Proc Biol Sci. 2003 Jul 22;270(1523):1447–1454. [PMC free article] [PubMed]
  • Liebers D, Helbig AJ, de Knijff P. Genetic differentiation and phylogeography of gulls in the Larus cachinnans-fuscus group (Aves: Charadriiformes). Mol Ecol. 2001 Oct;10(10):2447–2462. [PubMed]
  • Lijtmaer Darío A, Mahler Bettina, Tubaro Pablo L. Hybridization and postzygotic isolation patterns in pigeons and doves. Evolution. 2003 Jun;57(6):1411–1418. [PubMed]
  • Paulo Octávio S, Jordan William C, Bruford Michael W, Nichols Richard A. Using nested clade analysis to assess the history of colonization and the persistence of populations of an Iberian Lizard. Mol Ecol. 2002 Apr;11(4):809–819. [PubMed]
  • Servedio Maria R, Saetre Glenn-Peter. Speciation as a positive feedback loop between postzygotic and prezygotic barriers to gene flow. Proc Biol Sci. 2003 Jul 22;270(1523):1473–1479. [PMC free article] [PubMed]
  • Slatkin M. Gene flow and the geographic structure of natural populations. Science. 1987 May 15;236(4803):787–792. [PubMed]
  • Templeton AR. Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol. 1998 Apr;7(4):381–397. [PubMed]
  • Turelli M, Barton NH, Coyne JA. Theory and speciation. Trends Ecol Evol. 2001 Jul 1;16(7):330–343. [PubMed]
  • Vigilant L, Stoneking M, Harpending H, Hawkes K, Wilson AC. African populations and the evolution of human mitochondrial DNA. Science. 1991 Sep 27;253(5027):1503–1507. [PubMed]
  • Wake DB. Incipient species formation in salamanders of the Ensatina complex. Proc Natl Acad Sci U S A. 1997 Jul 22;94(15):7761–7767. [PubMed]

Articles from Proceedings of the Royal Society B: Biological Sciences are provided here courtesy of The Royal Society