The roles of time and ecology in the continental radiation of the Old World leaf warblers (Phylloscopus and Seicercus)

Abstract

Many continental sister species are allopatric or parapatric, ecologically similar and long separated, of the order of millions of years. Sympatric, ecologically differentiated, species, are often even older. This raises the question of whether build-up of sympatric diversity generally follows a slow process of divergence in allopatry, initially without much ecological change. I review patterns of speciation among birds belonging to the continental Eurasian Old World leaf warblers (Phylloscopus and Seicercus). I consider speciation to be a three-stage process (range expansions, barriers to gene flow, reproductive isolation) and ask how ecological factors at each stage have contributed to speciation, both among allopatric/parapatric sister species and among those lineages that eventually led to currently sympatric species. I suggest that time is probably the critical factor that leads to reproductive isolation between sympatric species and that a strong connection between ecological divergence and reproductive isolation remains to be established. Besides reproductive isolation, ecological factors can affect range expansions (e.g. habitat tracking) and the formation of barriers (e.g. treeless areas are effective barriers for warblers). Ecological factors may often limit speciation on continents because range expansions are difficult in 'ecologically full' environments.

Figure 1.

Numbers of Phylloscopus and Seicercus species in sympatry across continental Eurasia, as estimated by overlapping the range maps in Clement et al. (2006). Figure kindly constructed by B. Hawkins.

Figure 2.

Phylogenetic relationships among all species of continental Eurasian Old World leaf warblers (Seicercus and Phylloscopus) from Johansson et al. (2007), with non-continental taxa pruned. The tree was built using both mitochondrial and nuclear genes and rate-smoothed. Time scale at the bottom is based on a mitochondrial DNA rate of evolution of 2% Myr⁻¹, as assessed by comparing the average (GTR-γ corrected) distance in mtDNA cytochrome b across the root of the tree. Numbers on the tree indicate lineages at 4 Ma, and numbers to the right of the tree the percentage of the total geographical range that is shared, for couplets of species separated by less than 4 Myr, based on ranges in Clement et al. (2006), with some corrections. Possible overlap of borealis with its sister and forresti with chloronotus is unreported, but they are considered allopatric here. If no number is indicated, the couplets are allopatric. Dashed lines indicate continental taxa not considered by Johansson et al. (2007), which have been inserted based on information from the following: unnamed sister to Phylloscopus borealis (Saitoh et al. 2006; Reeves et al. 2008), Phylloscopus nitidus (Price et al. 1997), Phylloscopus forresti (Martens et al. 2004), Phylloscopus occisinensis (Martens et al. 2008), P. ibericus (Helbig et al. 1996) and Phylloscopus neglectus (U. Olsson & P. Alström, mtDNA cytochrome b sequence provided 2009, personal communication).

Figure 3.

Five of the six recognized species in the Seicercus burkii complex. Three of the illustrated species (Seicercus soror, S. tephrocephalus, Seicercus valentini) are common along a single altitudinal gradient in Emei Shan, China, with S. soror at the lowest elevations and S. valentini at the highest elevations. Seicercus burkii (lower) and Seicercus whistleri (higher) occur together in the Himalayas. Illustration drawn by Ian Lewington to accompany the article ‘The Golden spectacled warbler: a complex of sibling species, including a previously undescribed species’, by Alström & Olsson (1999).

Figure 4.

The chiffchaff (P. collybita) superspecies complex (redrawn from Martens 1996, after Helbig et al. 1996). Phylloscopus sindianus includes lorenzii as a subspecies; P. collybita includes tristis, abietinus and caucasicus. The complex includes (a) the only known hybrid zone in the Phylloscopus, (b) a large zone of introgression between two subspecies, and (c) possibly another contact zone. In addition, P. sindianus lorenzii and P. collybita caucasicus co-occur apparently without interbreeding in the Caucuses (Martens 1982). Adapted from illustration drawn by Emiko Paul for the book ‘Speciation in Birds’ by T. Price (2008, Roberts and Company).

Figure 5.

Association of the number of species in a lineage with the area covered by the lineage. Numbers by points refer to numbers on the lineages crossing the 4 Ma timeline as indicated in figure 2. Least squares trend line is drawn for illustration only. Significance was tested assuming Poisson errors with a log link, first using GLM in the statistical package R (p = 0.05), and second after correcting for phylogeny, based on the branch lengths of the truncated tree and using generalized estimating equations (Paradis & Claude 2002) implemented in APE (Paradis et al. 2004) (p = 0.01). When the mid-point of the latitudinal extent was included as a covariate, the corresponding p-values are p = 0.1 and p = 0.03, respectively.

Figure 6.

Phylogenetic relationships for species in two local communities, drawn on to the tree of figure 2. (a) Western Himalayas (34° N, 75° E; Price 1991). Note that Phylloscopus xanthoschistos was not in the paper of Price (1991), because this species occurs at lower, unstudied, elevations than the other species. (b) Central Siberia (62° N, 89° E; Forstmeier et al. 2001). One species (P. trochiloides viridanus) is held in common. Ecological categories for the three main clades are consistent across the Himalayan and Siberian studies. Flycatching versus picking refers to the extent to which prey capture involves a flying movement. Within each community, both the span of average feeding methods and body sizes among species within a clade do not overlap across the three clades.