Overview: Circular overlaps: Rare demonstrations of speciation

The perfect demonstration of speciation is presented by the situation in which a chain of intergrading sub-- species forms a loop or an overlapping circle, of which the terminal forms no longer interbreed, even though they coexist in the same localities. (Mayr 1942:180)

THE SPLITTING OF a single species into two or more is a difficult process to observe, because it can take a great deal of time. Evolutionary biologists have recognized that a solution to this problem is to use geographical variation to infer how change in time might occur. Especially interesting in that regard is the phenomenon of "circular overlaps" (Mayr 1942), or "ring species" (Cain 1954), in which two sympatric and clearly distinct forms are connected by a chain of populations through which the characteristics of one form gradually change into those of the other. The possibility that ring species might exist was first suggested about a century ago by Stejneger (as quoted by Jordan 1905), and since then a number of possible examples have generated intense interest among evolutionary biologists.

One of the most widely known of the proposed examples of ring species is the series of taxa in the Herring Gull (Larus argentatus) and Lesser Black-backed Gull (L. fuscus) group (Crochet et al. 2002). Ever since Mayr (1940, 1942) described these gulls as a prime example of circular overlap and geographic speciation, they have figured prominently in university course lectures, textbooks (e.g. Ridley 1993), and popular books on evolution (e.g. Schilthuizen 2001). The usual description follows from Mayr's writings:

The races of this species are arranged in a circumpolar ring, but Larus argentatus, coming from America, invaded western Europe and lives now side by side with Larus fuscus, like a good species, although the two "species" are connected by a chain of intermediate forms in Siberia and North America. (Mayr 1940:272)

Those conclusions were based primarily on morphological variation. The two supposedly terminal forms, which overlap in distribution in Europe, differ in size, shape, and plumage color, but those traits gradually change through the chain of forms encircling the Arctic Ocean. In the 60 years since Mayr first popularized that apparent example of ring speciation, evidence has accumulated that the relationships and history of the many taxa within the group are far more complicated than originally believed (reviewed by Mayr 1963, 1970; Grant 1982; Harrison 1985; Burger and Gochfeld 1996). There are many taxa in the group that are outside of the main ring, and there are complex patterns of reproductive isolation and hybridization. According to Burger and Gochfeld (1996:609), "systematics of [L. argentatus] and its close relatives represent one of the most complex challenges in ornithology, and typify the discord between evolution, biogeography, reproductive isolation, and taxonomy."

A number of researchers have examined molecular variation from parts of the Larus species complex in the hope of clarifying historical relationships between taxa and current patterns of gene flow (Ryttman et al. 1980, Johnson 1985, Snell 1991, de Knijff et al. 2001, Liebers et al. 2001, Crochet et al. 2002). The study by Crochet et al. (2002) is notable because it is the first molecular study to include samples from all of the taxa that had been considered part of the circumpolar ring species. The mitochondrial DNA variation revealed by Crochet et al. (2002) will be of prime relevance to studies of gull taxonomy, historical biogeography, and speciation. Perhaps most importantly, their results call into question an important element of the standard ring species description of the complex, that the European forms of Herring Gull (including the two taxa L. argentatus argenteus in northwestern Europe and L. argentatus argentatus in Scandinavia; for taxonomic names we follow Burger and Gochfeld [1996]) are closely related to and derived from the North American form of Herring Gull (L. argentatus smithsonianus). Instead, their results suggest that North American smithsonianus is more distantly related to the European forms Herring Gull (L. argentatus argenteus and L. argentatus argentatus) than is the European Lesser Black-backed Gull (L. fuscus). It appears that smithsonianus is highly related to a group of several other morphologically divergent species, such as Thayer's Gull (L. thayeri), Glaucous Gull (L. hyperboreus), Iceland Gull (L. glaucoides), Slaty-backed Gull (L. schistisagus), and California Gull (L. californicus), most of which are also found primarily in North America. These results lead Crochet et al. (2002) to suggest that smithsonianus, which is usually treated as a subspecies of L. argentatus (e.g. Harrison 1985, Burger and Gochfeld 1996), should be treated as its own species, Larus smithsonianus. Crochet et al. (2002) caution that this conclusion should be confirmed with higher sample sizes (they included nine smithsonianus samples from two sites), but for the time being their results call into question the theory that European L. argentatus resulted from a circumpolar expansion and gradual divergence of L. fuscus.