Effects of Pleistocene climatic fluctuations on the phylogeographic and demographic histories of Pacific herring (Clupea pallasii)

Jin‐Xian Liu,John C Avise,Andrey Tatarenkov,Sharon Wildes,Terry D Beacham,Victor Gorbachev

doi:10.1111/j.1365-294x.2011.05213.x

Abstract

We gathered mitochondrial DNA sequences (557 bp from the control region in 935 specimens and 668 bp of the cytochrome b gene in 139 specimens) of Pacific herring collected from 20 nearshore localities spanning the species' extensive range along the North Pacific coastlines of Asia and North America. Haplotype diversity and nucleotide diversity were high, and three major phylogeographic lineages (sequence divergences ca. 1.5%) were detected. Using a variety of phylogenetic methods, coalescent reasoning, and molecular dating interpreted in conjunction with paleoclimatic and physiographic evidence, we infer that the genetic make-up of extant populations of C. pallasii was shaped by Pleistocene environmental impacts on the historical demography of this species. A deep genealogical split that cleanly distinguishes populations in the western vs. eastern North Pacific probably originated as a vicariant separation associated with a glacial cycle that drove the species southward and isolated two ancestral populations in Asia and North America. Another deep genealogical split may have involved either a vicariant isolation of a third herring lineage (perhaps originally in the Gulf of California) or it may have resulted simply from the long coalescent times that are possible in large populations. Coalescent analyses showed that all the three evolutionary lineages of C. pallasii experienced major expansions in their most recent histories after having remained more stable in the preceding periods. Independent of the molecular calibration chosen, populations of C. pallasii appear to have remained stable or grown throughout the periods that covered at least two major glaciations, and probably more.

Highlights

The Pleistocene epoch was dominated by repeated episodes of global cooling and an expansion of continental ice sheets across much of North America and Eurasia (Lambeck et al 2002)
Our results indicate that climatic fluctuations of the Pleistocene left decipherable genetic footprints on several phylogeographic and demographic facets of herring history
A deep division between mtDNA lineages in the western vs. eastern North Pacific probably registers vicariant population separations and subsequent range shifts associated with Pleistocene glacial cooling

Summary

Introduction

The Pleistocene epoch was dominated by repeated episodes of global cooling and an expansion of continental ice sheets across much of North America and Eurasia (Lambeck et al 2002). The glacial–interglacial cycles with their alternating configurations of ice sheets and shorelines caused pronounced fluctuations in sea surface temperature (CLIMAP 1981; Herbert et al 2001; Lyle et al 2001) and in oceanic salinity, upwelling intensity and primary production (Sancetta & Silvestri 1984; Sancetta et al 1992; Herbert et al 2001; Marret et al 2001) All of these and related environmental factors must have had huge impacts on the distribution and abundance of marine species in the North Pacific region (Fields et al 1993; Roy et al 1996; Graham et al 2003). The nature of biogeographic responses to glaciation probably has varied considerably among taxa (Arndt & Smith 1998; Marko 2004; Hickerson & Cunningham 2005), with some species likely ‘floating’ with their habitats as the latter shifted across latitudes but with other species remaining more stationary as they adapted to their altered local environments (Marko et al 2010)

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Results

Discussion

Conclusion