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Rev Iss Web Jbi 12765 43-9 1728..1738 Journal of Biogeography (J. Biogeogr.) (2016) 43, 1728–1738 ORIGINAL Whole mitochondrial genomes ARTICLE illuminate ancient intercontinental dispersals of grey wolves (Canis lupus) Stephan Koblmuller€ 1,2, Carles Vila1, Belen Lorente-Galdos3, Marc Dabad3, Oscar Ramirez3, Tomas Marques-Bonet3, Robert K. Wayne4 and Jennifer A. Leonard1* 1Conservation and Evolutionary Genetics ABSTRACT Group, Estacion Biologica de Donana~ (EBD- Aim Grey wolves (Canis lupus) are widespread across the Holarctic. Here, we CSIC), 41092 Sevilla, Spain, 2Institute of test the previously proposed hypothesis that extant North American wolves Zoology, University of Graz, Universit€atsplatz 2, A-8010 Graz, Austria, 3ICREA, Institut de originate from multiple waves of colonization from Asia. We also test the Biologia Evolutiva (CSIC-UPF), Dr. Aiguader hypothesis that land connections have been important in the evolutionary 88, 08003 Barcelona, Spain, 4Department of history of other isolated wolf populations in Japan. Ecology and Evolutionary Biology, University Location Holarctic. of California, Los Angeles, CA 90095-1606, USA Methods We analyse 105 previously published and newly obtained complete mitochondrial genomes from a geographically diverse sample of grey wolves and date critical branches in the phylogenetic tree. Phylogeographical hypothe- ses are tested in an approximate Bayesian computation approach. Results We find that the mitogenomes of all living wolves in North America, including Mexican wolves, most likely derive from a single colonization event from Eurasia that expanded the grey wolf range into North America. This colo- nization occurred while a land bridge connected Eurasia and North America before the Cordillerian and Laurentide ice sheets fused in the Last Glacial Max- imum, c. 23 ka, much more recent than predicted based on the fossil record. Pleistocene land bridges also facilitated the separate colonization of Hokkaido and the southern Japanese islands. Main conclusions Extant wolf lineages in North America derive from wolves that migrated into North America coincident with the formation of the most recent land bridge with Eurasia. The maternal lineages from earlier Pleistocene American wolves are not represented in living American wolves, indicating that they left no descendants. The timing of colonization of North America, Hok- kaido and the southern Japanese islands corresponds to the changes in land connectivity as a consequence of changing sea level. *Correspondence: Jennifer Leonard, Conservation and Evolutionary Genetics Keywords Group, Estacion Biologica de Donana~ Beringia, canid, carnivore, mitogenome, molecular dating, Pleistocene (EBD-CSIC), 41092 Sevilla, Spain. E-mail: [email protected] dispersal smaller North American endemic canid. The fossil record INTRODUCTION supports the first appearance of wolves in Eurasia in the The grey wolf (Canis lupus L. 1758) is the largest canid and, early to mid-Pleistocene, 1–2.5 Ma, and then in North together with the red fox (Vulpes vulpes L. 1758), the most America in the mid-Pleistocene (Kurten, 1968; Tedford et al., widely distributed wild carnivoran. The species is found 2009). throughout the Holarctic from the High Arctic to the deserts The discovery of distinct phylogeographical patterns has of the Middle East and southern North America, but was been elusive in grey wolves. Early large-scale mitochondrial historically extirpated from parts of its original distribution, DNA studies found little support for large-scale patterns, and such as Japan and much of North America and Europe. It is revealed instead a polyphyletic ancestry of North American most closely related to the coyote (Canis latrans Say 1819), a wolves within the diversity of Eurasian wolves. However, 1728 http://wileyonlinelibrary.com/journal/jbi ª 2016 John Wiley & Sons Ltd doi:10.1111/jbi.12765 Dating intercontinental dispersals in grey wolves critical early branching events in the phylogenetic trees were c. 130 ka and so is too ancient to be consistent with mito- poorly supported (Wayne et al., 1992; Vila et al., 1999; Leo- chondrial DNA sequence data. From c. 24–13 ka, the fusion nard et al., 2005; Pilot et al., 2010; Thalmann et al., 2013). of the Laurentide with the Cordilleran ice sheet prevented The somewhat divergent haplotypes restricted to Mexican gene flow between Beringia (and hence Eurasia) and conti- wolves (C. l. baileyi) were hypothesized to represent an early nental North America (e.g. Burns, 2010; Gowan, 2013; invasion of wolves into North America (Wayne et al., 1992; Rabassa & Ponce, 2013). After the ice sheets started to retreat Leonard et al., 2005; Thalmann et al., 2013). Later research (c. 13 ka), the Yukon corridor opened and potentially based on nuclear loci suggested monophyly of North Ameri- allowed for dispersal between Eurasia and continental North can grey wolves (vonHoldt et al., 2011). Despite considerable America until the Bering Strait closed in the wake of rising genetic research on grey wolves, it is still not clear when they sea levels c. 10 ka, finally preventing intercontinental colonized North America, or if there have been subsequent migration of grey wolves. We used this historic and geo- gene flow or colonization events. The mid-Pleistocene record graphical framework to assess if the extant diversity of Amer- of grey wolves in North America reveals a long, complex his- ican wolves is best explained by a single or multiple tory. Conceivably, first colonization occurred during a period colonization(s) from Eurasia and to date the arrival of mod- of significantly lowered global sea levels when the Bering ern wolves to North America. land bridge was exposed and connected Asia to America, which occurred repeated during the Pleistocene and facili- MATERIALS AND METHODS tated colonization of America by Eurasian terrestrial verte- brates (e.g. Brunhoff et al., 2003; Davison et al., 2011; Mitochondrial genomes Kutschera et al., 2013). The Bering land bridge was not a narrow strip as the word ‘bridge’ may suggest, but covered We analysed 105 sequences of the 12 protein coding genes an area of over one and a half million square kilometres and located on the H-strand of the mitochondrial genome of incorporated some present-day islands, such as Wrangel grey wolves distributed across Eurasia and North America, Island. The same fluctuations in sea level that exposed the but excluding the divergent lineages from India and the Bering land bridge between Asia and North America Himalayas (Sharma et al., 2004; Aggarwal et al., 2007) also exposed other land bridges connecting, for example, (Table 1). Among the studied sequences we included 10 Hokkaido and the southern Japanese islands to mainland from ancient (> 14,000 years old) Eurasian and North Amer- Asia, allowing the expansion of wolves into these islands, ican wolves from Thalmann et al. (2013). Thirty-five new where they survived until the beginning of the 20th century mitogenomes from modern wolves were generated for this (Matsamura et al., 2014). study, either Sanger sequenced following Bjornerfeldt€ et al. Here, we analyse new and previously published mitogen- (2006) (n = 24) and aligned by eye in Mega 6.05 (Tamura omes of ancient and modern grey wolves from throughout et al., 2013), or reconstructed from whole-genome shotgun their distribution to assess large scale phylogeographical pat- (WGS) sequencing (n = 11). terns and statistically evaluate alternative scenarios regarding For each WGS sample, we captured mitochondrial reads the colonization of North America by means of an approxi- from the whole set of sequenced reads by mapping the raw mate Bayesian computation (ABC) approach. The timeframe data against a reference wolf mitochondrial genome tested was constrained by the time-calibrated genealogy and (DQ480508, Bjornerfeldt€ et al., 2006). We took advantage of reconstructions of Quaternary sea levels and the extent of ice the circularity of mtDNA in order to increase the number of sheets during the Last Glacial Maximum (LGM) (Siddall captured reads at the extremes of the assembly. With this et al., 2003; Miller et al., 2005; Rabassa & Ponce, 2013). The goal in mind, we applied a second round of mapping and total time period considered extends to the time of the most aligned the reads to a modified sequence assembly, changing recent common ancestor for all of the wolf mitogenomes the origin of the reference assembly at the middle of the (80 ka; Thalmann et al., 2013) and is much more recent mtDNA (8 kbp from the start). To map, we used BWA 0.6.1 than the time period suggested by the fossil record (Tedford aligner with parameters –n6–q 15 (Li & Durbin, 2009). We et al., 2009), but consistent with the recent divergence of kept only high-quality paired-end reads by retaining read Old World wolves suggested by nuclear data (Freedman pairs that both were mapped and properly paired and had a et al., 2014; Skoglund et al., 2015). Consequently, we mapping quality > 50 (with samtools 0.1.18 –f2–q 50; Li hypothesize that because colonization of North America was et al., 2009). We discarded paired-end pairs if at least one of only possible during periods when the Bering land bridge both paired-ends had a median Phred quality score < 32. was present, it must have occurred during the last emergence We used Hapsembler 1.1. (-p Illumina -t 4 -d no –PHRE- of the Bering land bridge (Fig. 1). The average water depth D_OFFSET 33 –MIN_CONTIG_SIZE 1000 –EPSILON 0.05) of the Bering Strait is 40–50 m. The land bridge was likely (Donmez & Brudno, 2011), a haplotype-specific genome open when the sea level dropped more than 50 m below the assembly toolkit, to construct longer sequences from multiple current level, with a minimum relative sea level (c. À140 m) overlapping reads (contigs) from the captured reads. The at the LGM, 20 ka (Siddall et al., 2003; Miller et al., 2005). elevated mitochondrial coverage, calculated from the cap- The penultimate emergence of the land bridge was about tured high-quality reads, decreases the efficiency of the Journal of Biogeography 43, 1728–1738 1729 ª 2016 John Wiley & Sons Ltd S.
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