Evolutionary genetics: A ring of species
A long-standing model illustrating how new species can arise through ‘circular overlap’, without interruption of gene flow through intervening populations, has now been confirmed among passerine birds (Irwin et al, 2005). The new study of the Eurasian greenish warbler (Phylloscopus trochiloides) complex shows that reproductive isolation, the hallmark of biological species, can arise through ‘isolation-by-distance’ (Slatkin, 1993), such that large distances themselves restrict gene flow. The question of how species arise, the ‘mystery of mysteries’ as Darwin put it, has received much recent attention (Coyne and Orr, 2004). Birds have featured prominently as subjects in speciation research, in particular, illustrating the classic allopatric model of speciation through geographic separation. The recently deceased Ernst Mayr, one of the most outspoken proponents of the allopatric speciation model, was also the first to outline clearly a nonallopatric alternative, which he called ‘speciation by circular overlap’ (see Figure 1). This intuitively plausible idea actually goes back to the German biologists Bernhard Rensch and Geyr von Schweppenburg and was based on their observations of the Great Tit (Parus major) complex in Eurasia and the circumpolar Herring Gull (Larus argentatus) group, respectively. However, when these and other potential ‘ring species’ like the Ensatina salamanders of western North America were studied in detail (Wake, 1997; Kvist et al, 2003; Liebers et al, 2004), the allopatric divergence model seemed to explain the genetic data better than the ring species model did. In most cases, fragmentation of ranges, and thus divergence in geographic isolation, has happened at some point before the circular range around an uninhabitable barrier closed. This is not to say that isolation-by-distance was unimportant, but the crucial question remained whether it is sufficient to lead to reproductive isolation. This question has now been answered positively by Irwin and colleagues’ (2005) study of the greenish warbler complex, which provides the most convincing case to date in support of the ring species model. Greenish warblers are small, drab-looking songbirds living in forested habitats across much of Eurasia and around the Himalayan mountain system. It had been known for some time that north of the Tibetan plateau, a huge treeless desert uninhabitable to a forest-dwelling warbler, there are two forms of greenish warbler that differ in plumage and song, but do not interbreed (viridanus in the west, plumbeitarsus in the east). These populations coexist as distinct biological species in the Siberian lowlands, but are connected through an until recently contiguous breeding range all around the Central Asian mountains. Using amplified fragment length polymorphism markers to survey a large number of anonymous nuclear gene loci, Irwin and co-workers show that there is a genetic continuum throughout this ring-shaped range, except in the zone of overlap in Siberia, where genetic divergence reaches its maximum. The physical distance around the ring is about 9000 km, orders of magnitude larger than the distance an average young greenish warbler will travel from its birth place to its later breeding territory. Genetic distance is strongly correlated with geographic distance throughout the ring of intergrading populations, except in the zone of overlap, where this correlation breaks down abruptly. Historically, this situation most likely arose when ancestors of today’s greenish warblers from a refugium somewhere south of the Himalayas spread northwards on both sides of the mountain range. Separated by larger and larger intervening distances, the peripheral populations diverged as they were exposed to different selection pressures leading to differences in morphology, plumage and song. All conditions specified by the ring species model are met: a contiguous ring-shaped range with genetic continuity throughout, but a sharp genetic break where the ring has closed. Two aspects are important in the warbler example that might distinguish it from other cases of potential ring species that have since been discredited. First, sexual selection is important in these songbirds, and it seems to be song characteristics that are most strongly selected by females when choosing a mate. This opens the door for a Fisherian run-away process in which different song parameters may be selected between geographically distant populations. True enough, song characteristics best distinguish the sympatric (overlapping) populations of viridanus and plumbeitarsus warblers in Siberia, although variation in song parameters, just like the genetic make-up of populations, was found to be continuous as one travels from the overlap zone