Return to Beringia: parasites reveal cryptic biogeographic history of North American pikas

Kurt E. Galbreath () 1 2 Eric P. Hoberg 0 0 Animal Parasitic Diseases Laboratory, United States National Parasite Collection , ARS USDA, BARC East 1180, Beltsville, MD 20705 , USA 1 Department of Biology, Western Washington University , Bellingham, WA 98225 , USA 2 Department of Ecology and Evolutionary Biology, Cornell University , Ithaca, NY 14853 , USA Traditional concepts of the Bering Land Bridge as a zone of predominantly eastward expansion from Eurasia and a staging area for subsequent colonization of lower latitudes in North America led to early inferences regarding biogeographic histories of North American faunas, many of which remain untested. Here we apply a host - parasite comparative phylogeographical (HPCP) approach to evaluate one such history, by testing competing biogeographic hypotheses for five lineages of host-specific parasites shared by the collared pika (Ochotona collaris) and American pika (Ochotona princeps) of North America. We determine whether the southern host species (O. princeps) was descended from a northern ancestor or vice versa. Three parasite phylogenies revealed patterns consistent with the hypothesis of a southern origin, which is corroborated by four additional parasite lineages restricted to O. princeps. This finding reverses the traditional narrative for the origins of North American pikas and highlights the role of dispersal from temperate North America into Beringia in structuring northern diversity considerably prior to the Holocene. By evaluating multiple parasite lineages simultaneously, the study demonstrates the power of HPCP for resolving complex biogeographic histories that are not revealed by characteristics of the host alone. 1. INTRODUCTION Beringia, the region spanning eastern Siberia and northwestern North America, played a central role in structuring Holarctic biotas, and the biogeographic history across this province has consequently been the subject of intense scrutiny [1 4]. The Bering Land Bridge was an intermittent terrestrial corridor that facilitated bi-directional dispersal between the northern continents through much of the Tertiary. With the onset of episodic glaciations during the Pliocene and Pleistocene, faunal expansion across the region became increasingly asymmetrical as greater numbers of Eurasian species colonized eastern Beringia and the Nearctic [5,6]. As a result, during Quaternary interglacials, temperate latitudes of North America were frequently colonized from source populations of species that were first established in Beringia. However, a reciprocal influence for low-latitude faunas relative to Beringian diversity is not well documented. There are relatively few clear cases of deep (Pliocene or Pleistocene) expansion into Beringia by temperate North American species that then survived in the north through subsequent glacial stages. The colonization of Eurasia by North American equids and camelids provides classic examples [6], and more recent phylogenetic work has revealed evidence for similar histories in some small mammals [7,8]. Although numerous instances of post-glacial (Holocene) range expansion from southern refugia have been described, some of which involve species that successfully invaded Beringia [4,9], the role of such events (or analogous events during previous interglacials) in establishing new and persistent northern lineages has not been fully demonstrated. Early ideas about North American faunal history were strongly influenced by the observation that colonization across Beringia over the past few million years was dominated by Asian immigrants entering North America [10]. Many hypotheses viewed Beringia as an engine of diversity for descendant components of North American faunas. Critical evaluation of these concepts is increasingly warranted in light of more contemporary perspectives on the complexities of Beringian biogeography [4,9]. Pikas, small lagomorphs of the genus Ochotona, provide a case in point. Pikas originated in the Palearctic and colonized the Nearctic via Beringia. The two extant North American species are sister [11,12], with the collared pika (Ochotona collaris) occurring in Alaska and adjacent Canadian provinces and the American pika (Ochotona princeps) distributed across North Americas Intermountain West (figure 1). Based on their Old World origin and geographical distribution in North America, it was suggested that the northern O. collaris evolved directly from the ancestral Beringian colonizers, while O. princeps originated from individuals that expanded southward along the Coastal and Rocky Mountains of western North America [13]. However, evidence for this history is lacking. Indeed, pikas that are morphologically consistent with the extant species appear earlier in the fossil record at low latitudes (c) North-to-South (d) (approx. 850 000 years before present; kyBP) than at high latitudes (,300 kyBP) [14], raising the alternative hypothesis that the ancestral northern population did not persist, and that O. collaris is descended from a southern ancestor. Under either scenario, speciation probably occurred when continental ice sheets isolated northern and southern populations [13]. The two mutually exclusive hypotheses make different phylogenetic predictions. The North-to-South (N S) hypothesis assumes that North American colonization proceeded from Siberia to Alaska and eventually to lower latitudes, resulting in southern diversity nested within the northern clade (figure 1). Conversely, if O. collaris is derived from a southern ancestor (South-to-North; S N), we would predict southern paraphyly. Under either scenario, northern and southern populations could be reciprocally monophyletic given sufficient time for lineage sorting to occur. Evidence from mitochondrial [12] and allozymic [15] data suggest that collared and American pikas are reciprocally monophyletic, providing no insight into the question of colonization history. In the absence of informative data from pikas themselves, we can test the alternative histories for North American Ochotona by applying a host parasite comparative phylogeographical (HPCP) approach. Parasites can be excellent indicators of host biogeographic and ecological histories [16], which can be illuminated using co-phylogenetic methods [17]. Similarly, comparative phylogeography offers a powerful approach for reconstructing regional biogeographic histories from comparisons of co-distributed taxa [18]. A natural union of these related fields has resulted in the development of the HPCP approach [19,20]. Many HPCP studies focus on single parasite lineages, making it impossible to distinguish between patterns that reflect the history of the full assemblage versus taxon-specific processes. The solution is to incorporate at least one additional taxon, representing an independent perspective on the history in question (the Threes Rule; [17]). Here, we demonstrate the power of HPCP analysis using multiple parasi (...truncated)