Shorter telomeres precede population extinction in wild lizards

Andréaz Dupoué,Sandrine Meylan,Jean François Le Galliard,Stéphanie Ruault,Alexis Rutschmann,Frédéric Angelier,Donald Miles,Coline Marciau,Jean Clobert

doi:10.1038/s41598-017-17323-z

Abstract

Identifying the early warning signals of catastrophic extinctions has recently become a central focus for ecologists, but species’ functional responses to environmental changes remain an untapped source for the sharpening of such warning signals. Telomere length (TL) analysis represents a promising molecular tool with which to raise the alarm regarding early population decline, since telomere attrition is associated with aging processes and accelerates after a recurrent exposure to environmental stressors. In the southern margin of their range, populations of the common lizard (Zootoca vivipara) recently became extinct at lowest elevations due to changes in climate conditions. However, the proximal signals involved in these demographic declines are still unknown. Here, we sampled 100 yearling lizards from 10 natural populations (n = 10 per population) along an extinction risk gradient. Relative lizard abundance dramatically dropped over 12 years in low-altitude populations characterized by warmer ambient temperatures and higher body growth of lizards early in life. A non-linear relationship was found between TL and population extinction risk, with shorter telomeres in populations facing high risk of extinction when compared to non-threatened ones. Our results identify TL as a promising biomarker and imply that population extinctions might be preceded by a loop of physiological aging.

Highlights

Anthropogenic activities lead to regime shifts and critical transitions in ecological systems at an unprecedented pace, including extinctions of an increasing number of species and for the future[1,2]
Correlates with thermal stress experienced by natural populations[28,29], and population extinction due to climate warming may be signalled by telomere loss
Mountain populations of the common lizard (Z. vivipara) recently went extinct at low altitudes in the southern, hot margin of the European range, and this has been directly correlated with a higher frequency of spells of warm and dry weather during the last two decades[32,34]

Summary

Introduction

Anthropogenic activities lead to regime shifts and critical transitions in ecological systems at an unprecedented pace, including extinctions of an increasing number of species and for the future[1,2]. Correlates with thermal stress experienced by natural populations[28,29], and population extinction due to climate warming may be signalled by telomere loss. A significant proportion of local lizard populations have been extirpated by climate warming worldwide during the last three decades[32,34,35] This is especially true in areas such as mountain or tropical ecosystems that associate strong endemism, and in which species are adapted to narrow thermal ranges[36,37]. Mountain populations of the common lizard (Z. vivipara) recently went extinct at low altitudes in the southern, hot margin of the European range, and this has been directly correlated with a higher frequency of spells of warm and dry weather during the last two decades[32,34]. We hypothesised that TL would correlate with population risk of extinction and predicted that shorter telomere should indicate population collapse

Methods

Results

Conclusion