THE TEMPO OF AVIAN DIVERSIFICATION: REPLY

The tempo of avian speciation, especially regarding the "importance" of Pleistocene events, is an ongoing and recently enlivened topic of discussion and debate (Lovette 2005). Klicka and Zink (1997) used molecular data from 48 pairs of North American songbird species, 35 of which were postulated to have differentiated during the two most recent glacial advances, to test the Late Pleistocene origins (LPO) model. Their results showed that "the majority of North America's 'youngest' species have Early Pleistocene or Late Pliocene origins" (Klicka and Zink 1997, p. 1668). Thus, they rejected the LPO model as a failed paradigm. Johnson and Cicero (2004) questioned their results because many of the species pairs chosen by Klicka and Zink for analysis were not sister taxa (24 [68.6%] of the 35 late Pleistocene pairs). Although earlier hypotheses about late Pleistocene origins for North American songbirds (e.g., Mengel 1964; Hubbard 1973) preceded modern molecular data, and thus were disadvantaged by the lack of known sisters, a suite of recent studies permitted reanalysis of sister-species pairs. Johnson and Cicero used the same methods as Klicka and Zink for 39 pairs of North American avian sister species, which "required exclusion of numerous species pairs used by [those authors] that subsequently have been shown to be non-sisters based on molecular data" (Johnson and Cicero 2004, p. 1123). Johnson and Cicero found the distribution of divergence values to be significantly different from that reported by Klicka and Zink, with only one pair of late Pliocene origin and the remainder skewed toward more recent times. Thus, Johnson and Cicero concluded that "the entire Pleistocene, including the last two glacial cycles (< 250,000 years ago), was important in speciations of modern North American birds" (Johnson and Cicero 2004, p. 1122). Zink and Klicka (2006) argued that Johnson and Cicero's conclusions are flawed because they did not test their distribution of sister-taxon divergences against a null model (note that Klicka and Zink also did not use a null model). Specifically, Zink and Klicka emphasized that a clear meaning of the term "important" is required, which they defined as being above some baseline diversification rate. They tested the data of Johnson and Cicero against a "distribution of sister-taxon values derived from simulations based on a phylogenetic model of constant speciation-extinction rates" (their null model, using methods from Zink et al. 2004), and concluded that the distribution of values in Johnson and Cicero did not differ from random based on this null model. Thus, they stated: "If 'important' is taken to mean 'above some baseline rate', Johnson and Cicero's own data suggest that the late Pleistocene is no more important for speciation th n any other time during the last several million years." We pp eciate and agree that a null model is important in hypothesis testing, and support Zink and Klicka's (2006) and Zink et al.'s (2004) effort to provide null models for testing the tempo of avian diversification in North American birds. However, the null model posed by Zink and Klicka addresses a fundamentally different question from that investigated by Johnson and Cicero, both of which are useful for understanding avian evolutionary history. While the null model asks whether the distribution of sister-pair divergences differs from a model of constant diversification (i.e., equal rates of speciation and extinction), the data in Johnson and Cicero address the timing and duration of speciation by looking at the most recently diverged pairs of biologic species (for criteria for species analyzed, see Johnson and Cicero 2004, p. 1123). If the majority of modern biologic species diverged from their sister species in the late Pliocene or early Pleistocene, as suggested by Klicka and Zink, then speciation has had a "protracted history . .. throughout the Pleistocene and Pliocene" (Klicka and Zink 1997, p. 1667). However, if these divergences were initiated primarily during the Pleistocene (including midto late Pleistocene), as indicated by Johnson and Cicero, then conclusions about Pleistocene speciation in North American birds are fundamentally shifted in two "important" ways: (1) the typical duration of speciation is significantly shorter than suggested by Klicka and Zink (often as little as 250,000 yrs); and (2) a considerable number of extant biologic species began forming during the Pleistocene, contrary to the findings of Klicka and Zink. Thus, although Zink and Klicka's (2006) test of the null model does not reject their hypothesis of constant speciation/extinction rates, it does not negate the findings of Johnson and Cicero regarding the timing of origin of modern North American bird species. Zink and Klicka's (2006) test of the null model also does not explain the striking difference in distribution plots and average divergence times between the two studies (Klicka and Zink, mean = 5.1%; Johnson and Cicero, mean = 1.86%; Kolmogorov-Smirnov test, P < 0.001). This discrepancy is explained best by differential selection of species pairs in the respective analyses (including non-sisters in Klicka and Zink and new data in Johnson and Cicero 2004). Zink and Klicka emphasized that sampling sister taxa should be based on reciprocal monophyly of mitochondrial DNA (mtDNA) hapl types (Zink et al. 2004), irrespective of whether the pairs are classified as phylogroups, subspecies, or species. In contrast, Johnson and Cicero emphasized sister pairs that are at or near the boundary of biologic species. Ultimately, the 2 Ned K. Johnson passed away on June 11, 2003.