Allopatric speciation appears to be the dominant geographic mode of speciation in birds (Mayr 1942; Cracraft 1982; Chesser and Zink 1994; Friesen and Anderson 1997; Barraclough and Vogler 2000; Coyne and Price 2000; Drovetski 2003; Phillimore et al. 2008; Price 2008). Sympatric speciation is infrequent and generally associated with unusual reproductive circumstances. For example, African indigobirds (Vidua spp.) that parasitize nests of estrildid finches (Estrildidae) could have diverged sympatrically through host specialization (Sorenson et al. 2003). But overall, nest parasitism is uncommon across avian lineages, with host-specificity in parasitism and, therefore, the possibility for sympatric speciation being even less common. In the band-rumped storm-petrel (Oceanodroma castro), populations on several Atlantic archipelagos diverge due to breeding allochrony with birds breeding in different seasons in the same archipelago being evolutionary sister-units (Friesen et al. 2007). However, allochrony is not common in birds, even among other storm-petrels.
The intriguing question then is what conditions (if any) can facilitate sympatric speciation in birds? Adaptive radiation appears to be a likely scenario for sympatric speciation. However, studies of avian adaptive radiations on oceanic islands provide virtually no support for sympatric speciation (Coyne and Price 2000). In the Hawaiian honeycreepers (Drepanidinae), only 2 of 7 sister pairs occur on the same island – the Nihoa (Telespiza ultima) and Laysan (T. cantans) finches on Laysan, and the apapane (Himatione sanguinea) and akohekohe (Palmeria dolei) on Maui (Lerner et al. 2011). In both pairs, one species has a much wider distribution in the archipelago than the other, so the potential for allopatric speciation cannot be excluded. In the Galapagos Islands, all mockingbird lineages are allopatric (Arbogast et al. 2006) and for Darwin's finches, allopatry is proposed as the initial stage of speciation (Petren et al. 2005).
In adaptive radiations on continental landmasses, there is also little support for sympatric speciation. In grouse (Tetraoninae), a recently evolved Holarctic subfamily with many widely distributed, sympatric species and numerous adaptive physiological and morphological characters (Johnsgard 1983; Drovetski et al. 2006), peripatric speciation (divergence of a small peripheral population) appears to be the predominant mode of speciation (Drovetski 2003). In songbirds, molecular phylogenetic studies have shown that co-distributed species within Palearctic regions are the result of multiple colonizations of those regions or post vicariant (allopatric) range expansion, rather than the result of in situ (sympatric) speciation (Voelker 1999, 2002; Johannson et al. 2007; Voelker 2010).
The diversity of habitats along environmental gradients is thought to provide an opportunity for sympatric speciation to occur. Mountain areas are good examples of sharp elevational habitat gradients. Furthermore, mountain areas are known hot spots of avian diversity and endemism (Myers et al. 2000; Orme et al. 2005). However, the potential link between speciation across sharp elevational gradients and high avian endemism and diversity is not well supported. Studies in the mountains of South and Central America, hosting the richest avian diversity in the world, show that closely related lineages (e.g., sister taxa) are not found in different habitats along elevational gradients as would be expected under a sympatric speciation model. Instead, they are found in similar environments on different parts of single mountain ranges or on different ranges (Chaves and Smith 2011; Barrera-Guzmán et al. 2012; Gutiérrez-Pinto et al. 2012); these patterns suggest allopatric divergence. A similar pattern occurs in Africa, where studies of a variety of lineages (avian and non-avian) indicate that sister taxa are not co-distributed on single mountains (Voelker et al. 2010). While support for sympatric speciation in birds remains elusive, studies of montane-distributed groups which occupy different habitats may still provide the best opportunity to identify cases of ecological divergence supportive of sympatric speciation.
The Palearctic passerine family, Prunellidae (accentors; Fig. 1), provides such an opportunity. This family consists of a single genus (Prunella) comprising 13 species (Dickinson 2003), all of which are associated with mountains and none are long-distance migrants (Hatchwell 2005). Most accentors occur in the Himalayan region, broadly defined to include the Himalayas, Tibet, and mountains of south-central China east of Tibet, or in the central Palearctic (Fig. 2). Three species (rubiculoides, immaculata, and strophiata) are endemic to the Himalayan region, two (atrogularis and koslowi) are endemic to central Palearctic mountains, and two (fulvescens and himalayana) are distributed across these two regions (Fig. 2). Three species (fagani, modularis, and ocularis) are restricted to the western Palearctic. One (rubida) is endemic to Japan and Kuril islands, montanella is distributed across central and eastern Palearctic, and collaris is distributed across all regions (Fig. 2).
Importantly for an assessment of possible sympatric speciation in montane systems, habitat associations among accentors vary along an elevational gradient, from high alpine to lower montane forest habitats. Four of the thirteen species (montanella, koslowi, rubida, and modularis) can also be found in lowlands.
This variation in habitat associations has been used taxonomically, with some authors subdividing Prunella into two subgenera or genera: Laiscopus and Prunella (Stepanyan 2003; Hatchwell 2005). Laiscopus includes two larger species (collaris and himalayana), which breed in alpine habitats, while Prunella includes the remaining 11 species, all of which are smaller than Laiscopus and associated with shrub habitats inside forest or adjacent habitats. The Himalayas and south-central Siberian regions are each inhabited by both of the Laiscopus species and by four Prunella, suggesting the possibility that speciation in these regions resulted from ecological divergence (sympatric speciation) rather than geographic isolation (allopatric speciation).
Therefore, in this study we focused on the evolutionary relationships, biogeographic history, and geographic mode of speciation in Prunellidae. We used sequences of the mitochondrial ND2 gene and intron 9 of the Z chromosome specific Aconitase 1 gene (ACO1I9) to reconstruct a phylogeny of all currently recognized species in the family. This phylogeny is then utilized to reconstruct the biogeographic history of Prunellidae and to test whether these mountain specialists diverge in allopatry or in sympatry.