Pleistocene speciation in the genus populus (salicaceae)

Despite evidence for the influence of Pleistocene (1.8–0.12 Ma) climate change on patterns of intraspecific genetic variation (Hewitt 1996), there is no consensus regarding its importance for driving speciation (Bennett 2004; Futuyma 2010). For many lineages, especially those with long generation times (e.g., trees), fossil evidence indicates macroevolutionary stasis throughout the Pleistocene (Willis and Niklas 2004; Eldredge 2005). Explanations for this stasis include the relatively short duration of climate cycles, which are insufficient to result in species-level divergence (Bennett 1990), as well as the inhibition of species-wide phenotypic evolution encountered in a geographic mosaic (Eldredge et al. 2005). Evaluation of the stasis hypothesis is incomplete however, because the paleobotanical record is unable to assess lineage splitting without coincident morphological divergence. Despite the well-known history of climate change and glaciation in North America, no clear examples of Pleistocene-age tree speciation from temperate or boreal regions have been demonstrated. Computational, theoretical, and DNA sequencing advances of the last two decades provide the opportunity to integrate information on the timing of genome-wide divergence with patterns of historical range changes to understand past speciation events (Richards et al. 2007). Coalescent analyses of multilocus DNA sequence data allow estimation of the timing and demographic consequences of speciation, even for lineages with poor or no fossil record (Wakeley and Hey 1997). For recent divergence events, detailed estimates of species' historical distributions can also be inferred, allowing for the development of data-driven scenarios to understand processes underlying divergence (Knowles et al. 2007; Hickerson 2010). Populus balsamifera L. and P. trichocarpa Torr & Gray are relatively short-lived (≤200 years maximum life span), fast-growing, dioecious tree species that are capable of clonal growth and very long distance gene flow (Eckenwalder 1996). The species are among the best-understood North American trees with respect to patterns of nucleotide variation and physiology (Gilchrist et al. 2006; Soolanayakanahally et al. 2009; Dillen et al. 2010; Keller et al. 2010; Olson et al. 2010). Nevertheless, their history of divergence remains underexplored, despite their morphological similarity, close phylogenetic affinity, and natural hybrid formation ( Viereck 1970; Hamzeh and Dayanandan 2004; Eckenwalder 2010), which may indicate recent speciation. Both P. balsamifera and P. trichocarpa range into high latitudes of North America and are parapatric in Alaska and Canada with little distributional overlap (Fig. 1a,1b). The fossil record of western North America indicates that antecedents (e.g., P. eotremuloides; Fig. 1b) of this lineage occupied the Pacific Northwest since at least the late Oligocene (∼23 Ma) and were anatomically similar to P. trichocarpa (Axelrod 1988, 1998). Figure 1. Maps show (a) the current distribution of Populus balsamifera, (b) the current distribution of P. trichocarpa, and (c) the maximum extent of the Wisconsin glaciation (21 Ka) with prominent glacial refugia labeled. Species distributions are based on the ... Here we investigate the timing and geography of divergence between P. balsamifera and P. trichocarpa, 2 keystone species of the boreal and Pacific temperate forests, by coupling coalescent-based divergence time estimation with modeling of historical species distributions. Integrating these approaches allows data- and model-based inferences regarding the following questions: (i) was the divergence of P. balsamifera and P. trichocarpa temporally associated with a Pleistocene-age climatic event and (ii) if so, did the divergence coincide with climatically mediated shifts in the species distribution?