Clade extinction appears to balance species diversification in sister lineages of Afro-Oriental passerine birds

Recent analyses suggest that the number of species in a clade often increases rapidly at first, but that diversification subsequently slows, apparently as species fill ecological space. Support for diversity dependence comes largely from the failure of species richness to increase with clade age in some analyses of contemporary diversity. However, clades chosen for analysis generally are named taxa and thus are not selected at random. To avoid this potential bias, we analyzed the numbers of species and estimated ages of 150 pairs of sister clades established by dispersal of ancestral species between the Oriental and African biogeographic regions. The observed positive exponential relationship between clade size and age suggests that species diversify within clades without apparent limit. If this were true, the pattern of accumulation of sister-clade pairs with increasing age would be consistent with the random decline and extinction of entire clades, maintaining an overall balance in species richness. This “pulse” model of diversification is consistent with the fossil record of most groups and reconciles conflicting evidence concerning diversity dependence of clade growth.The close relationship between local species richness and characteristics of the physical environment supports the existence of ecological constraints on species coexistence mediated through competition and other interactions (1–3), although historical influences on diversity sometimes parallel gradients in the physical environment (4–6). If species richness were limited as ecological space filled, one would expect the net rate of species production to slow and the number of species in a clade to level off as species richness approached ecological constraints.Evidence for such “diversity-dependent diversification” consists mostly of (i) nonrandom concentrations of branch points (speciation events) toward the origin of a clade (7–12) and (ii) independence of the number of species and clade age in comparisons among clades (11–14). However, clades included in such analyses often are not randomly chosen. In particular, small clades may be ignored because they do not command interest, and large, older clades are often passed over because of incomplete sampling (15, 16). Moreover, most phylogenetic analyses of diversification include species in named higher taxa rather than clades that have diversified within particular regions.Further support for diversity limits comes from the fossil records of many higher taxa, which exhibit long-term stability in number of species (17–19). It is also clear that species and entire clades continually replace each other through time, and the dynamics of this process appear to include the decline and extinction of evolutionary groups as a component of the local and regional regulation of the number of coexisting species (20–25).We take advantage of the sister relationships of clades of passerine birds in two major biogeographic regions—tropical southern Asia [Oriental (OR)] and the continent of Africa [African (AF)]—to examine the independent diversification of sister clades of known stem ages, selected only because one of the ancestors had dispersed between the two continents at some time in the past. Movement of species between these regions occurred either over water across the Indian Ocean, possibly using island stepping-stones, or through the Arabian Peninsula during periods of suitable environment. Each dispersal event defines the origin of a pair of same-aged sister clades in the two regions.If each diversifying clade filled a certain part of ecological space to a carrying capacity for species, after which diversification slowed, the sizes of clades filling this space would level off over time (26). Furthermore, the number of species per sister clade, particularly among older clades that have filled ecological space, might be correlated between regions, with species richness reflecting the ecological space available to each of the sister lineages (27). Finally, for those dispersal events whose directionality can be inferred, the rate of diversification should be higher, leading to larger clade size compared between sister lineages, in the newly colonized region, which initially would have fewer close (and ecologically similar) relatives of the ancestral species.We include all species of passerine birds (Passeriformes) and, separately, species in nonpasserine orders, of small, terrestrial birds, in the Oriental and African biogeographic regions (SI Appendix, section S1). The passerine avifauna of these regions accumulated from several sources over most of the Cenozoic Era (28, 29), with an old Gondwanan clade of suboscine passerines diversifying in tropical Africa and southern Asia early in the Tertiary, followed by radiations of core corvoid and passerid oscine passerines out of Australia during the early to mid-Cenozoic, through Wallacea to southern Asia, or directly across the Indian Ocean to Africa (30, 31). Thus, the diversification of sister clades in the African and Oriental regions takes place against a background of an increasing number of lineages of modern passerine birds as a whole within the region. Nonpasserine orders of terrestrial birds are likely to have diversified earlier within these regions (32) and perhaps were replaced to some extent by the passerines.Characteristics of a sample of clades include the distribution of node ages and the relationship between clade size and stem age, as well as the distribution of clade sizes regardless of age, including the proportion of clades that contain a single species. Any process-based model of diversification should be judged by how well it reproduces these characteristics. We use these criteria to evaluate simulations in which we attempt to reconstruct the underlying diversification process.