Mitogenome evolution in the last surviving woolly mammoth population reveals neutral and functional consequences of small population size.

Patrícia Pečnerová,Love Dalén,David Díez-Del-Molino,Pontus Skoglund,Christopher W Wheat,Alexei Tikhonov,Sergey Vartanyan,Johannes Van Der Plicht,Eleftheria Palkopoulou,Pavel Nikolskiy

doi:10.1002/evl3.33

Abstract

The onset of the Holocene was associated with a global temperature increase, which led to a rise in sea levels and isolation of the last surviving population of woolly mammoths on Wrangel Island. Understanding what happened with the population's genetic diversity at the time of the isolation and during the ensuing 6000 years can help clarify the effects of bottlenecks and subsequent limited population sizes in species approaching extinction. Previous genetic studies have highlighted questions about how the Holocene Wrangel population was established and how the isolation event affected genetic diversity. Here, we generated high‐quality mitogenomes from 21 radiocarbon‐dated woolly mammoths to compare the ancestral large and genetically diverse Late Pleistocene Siberian population and the small Holocene Wrangel population. Our results indicate that mitogenome diversity was reduced to one single haplotype at the time of the isolation, and thus that the Holocene Wrangel Island population was established by a single maternal lineage. Moreover, we show that the ensuing small effective population size coincided with fixation of a nonsynonymous mutation, and a comparative analysis of mutation rates suggests that the evolutionary rate was accelerated in the Holocene population. These results suggest that isolation on Wrangel Island led to an increase in the frequency of deleterious genetic variation, and thus are consistent with the hypothesis that strong genetic drift in small populations leads to purifying selection being less effective in removing deleterious mutations.

Highlights

While most of the Pleistocene megafauna species became extinct at the end of the last ice age, the woolly mammoth survived in small insular populations, most notably on Wrangel Island where it survived until 4000 years before present
It is still unclear to what extent genetic diversity was lost as a consequence of a founder effect when rising sea levels led to the formation of the island, compared to the subsequent effect of small effective population size during the ensuing 6000 years
Our results show a severe loss in genetic diversity and fixation of a mutation with potential functional consequences at the time the population was established, supporting the hypothesis of a founder effect

Summary

Introduction

Evolution Letters published by Wiley Periodicals, Inc. on behalf of Society for the Study of Evolution 1 (SSE) and European Society for Evolutionary Biology (ESEB). While most of the Pleistocene megafauna species became extinct at the end of the last ice age, the woolly mammoth survived in small insular populations, most notably on Wrangel Island where it survived until 4000 years before present. Changes in environmental conditions can potentially lead to adaptation through selection on standing genetic variation. The woolly mammoth (Mammuthus primigenius) inhabited the Northern Hemisphere for ß800 thousand years (kyr), from the late Middle Pleistocene to early Holocene (Lister and Sher 2001). Mammoths survived a number of alternating glacials and interglacials, but went extinct during the Holocene interglacial period ß4 thousand years before present (kyr calBP) (Vartanyan et al 1995). The fossil record and strontium isotopes in bones indicate that mammoths were not permanent residents in the region during the Late Pleistocene, but rather visited (what later became) Wrangel Island during seasonal migrations (Vartanyan et al 2008; Arppe et al 2009)

Methods

Results

Conclusion