Rapid Diversification, Incomplete Isolation, and the “Speciation Clock” in North American Salamanders (Genus Plethodon): Testing the Hybrid Swarm Hypothesis of Rapid Radiation

Abstract

The history of life has been marked by several spectacular radiations, in which many lineages arise over a short period of time. A possible consequence of such rapid splitting in the recent past is that the intrinsic barriers that prevent gene flow between many species may have too little time to develop fully, leading to extensive hybridization among recently evolved lineages. The salamander genus Plethodon in eastern North America has been proposed as a possible example of this scenario, but without explicit statistical tests. In this paper, we present a nearly comprehensive phylogeny for the 45 extant species of eastern Plethodon, based on DNA sequences of mitochondrial (two genes, 1335 base pairs) and nuclear genes (two genes, up to 3481 base pairs). We then use this phylogeny to examine rates and patterns of diversification and hybridization. We find significantly rapid diversification within the glutinosus species group. Examining patterns of natural hybridization in light of the phylogeny shows considerable hybridization within this clade, including introgression between species that are morphologically distinct and distantly related. Reproductive isolation increases over time and may be very weak among the most recently diverged species. These results suggest that the origin of species and the evolution of intrinsic reproductive isolating mechanisms, rather than being synonymous, may be decoupled in some cases (i.e., rapid origin of lineages outstrips the "speciation clock"). In contrast to the conclusions of a recent review of adaptive radiation and hybridization, we suggest that extensive hybridization sometimes may be a consequence, rather than a cause, of rapid diversification.

Explosive Pleistocene diversification and hemispheric expansion of a “great speciator”

“…1). A conservative estimate of diversity in Clade B (80 species) and a Yule model of diversification yielded a diversification rate of 2.24 taxa per million years (CI, 1.95-2.63), which far exceeds most published estimates for speciose radiations (1,(3)(4)(5)(6)(7). For comparison, Weir and Schluter (22) estimated an average age of 3 million years for sister-species pairs of Neotropical birds, older than all of Clade B ( Fig.…”

“…D isparity in diversification rates among groups of organisms is well documented and provides unique opportunities for studying evolutionary processes underlying the genesis of biological diversity (1)(2)(3)(4)(5)(6)(7). A few groups of organisms that diversified recently and rapidly have contributed disproportionately to speciation theory by providing comparatively accessible opportunities to evaluate factors that drive speciation (1)(2)(3)(4).…”

Patterns of differential introgression in a salamander hybrid zone: inferences from genetic data and ecological niche modelling

“…The findings presented here have considerable potential to explain the patterns observed in other hybrid zones among Plethodon in the southern Appalachians. A rapid radiation leading to high species richness (Highton 1995;Wiens et al 2006) has resulted in myriad hybrid zones among Plethodon in the southeastern United States (Highton & Peabody 2000). Given the mountainous terrain encompassing the ranges of many of these species, the seemingly narrow climatic specificity of many high elevation Plethodon species (Kozak & Wiens 2006, and past oscillations in climate, we may reasonably expect many of these hybrid zones to be dynamic.…”

“…A more likely scenario is that repeated bouts of isolation and secondary contact (perhaps as early as eight million years ago, i.e. shortly after molecular clock estimates place the date of divergence; Highton 1995; Wiens et al 2006) have left a complex, mosaic pattern of hybridization. In addition, severely limited dispersal abilities (as suggested by small home range sizes; Madison & Shoop 1970;Merchant 1972;Nishikawa 1990), long generation times (every other year beginning at 4 years of age for P. jordani and P. metcalfi ;Hairston 1983) and stasis during the 18-year study period of Hairston et al (1992) suggest this hybrid zone, if moving, may be doing so very slowly.…”

Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds

“…Most microevolutionary research on speciation implicitly assumes that RI is the defining and rate-limiting step in the speciation process (7,8,11), but the evolution of RI need not bear any predictive relationship to rates of species diversification as realized over macroevolutionary timescales (12). This has long been recognized by the paleontological community, where "successful" speciation is believed to entail not only the evolution of reproductive isolation but also the persistence of incipient species (13)(14)(15).…”