Catastrophic Floods May Pave the Way for Increased Genetic Diversity in Endemic Artesian Spring Snail Populations

Jessica Worthington Wilmer,Lynde Murray,Ché Elkin,Hugh Possingham,Darren Niejalke,Chris Wilcox,Dirk Steinke

doi:10.1371/journal.pone.0028645

Jessica Worthington Wilmer, Lynde Murray + Show 5 more

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https://doi.org/10.1371/journal.pone.0028645

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Abstract

The role of disturbance in the promotion of biological heterogeneity is widely recognised and occurs at a variety of ecological and evolutionary scales. However, within species, the impact of disturbances that decimate populations are neither predicted nor known to result in conditions that promote genetic diversity. Directly examining the population genetic consequences of catastrophic disturbances however, is rarely possible, as it requires both longitudinal genetic data sets and serendipitous timing. Our long-term study of the endemic aquatic invertebrates of the artesian spring ecosystem of arid central Australia has presented such an opportunity. Here we show a catastrophic flood event, which caused a near total population crash in an aquatic snail species (Fonscochlea accepta) endemic to this ecosystem, may have led to enhanced levels of within species genetic diversity. Analyses of individuals sampled and genotyped from the same springs sampled both pre (1988–1990) and post (1995, 2002–2006) a devastating flood event in 1992, revealed significantly higher allelic richness, reduced temporal population structuring and greater effective population sizes in nearly all post flood populations. Our results suggest that the response of individual species to disturbance and severe population bottlenecks is likely to be highly idiosyncratic and may depend on both their ecology (whether they are resilient or resistant to disturbance) and the stability of the environmental conditions (i.e. frequency and intensity of disturbances) in which they have evolved.

Highlights

Despite the immediate and seemingly far reaching devastation that follows intense natural disturbances, there is an extensive literature showing that such events can generate environmental conditions favourable to the survival, growth and diversification of living organisms and ecosystems, at least as measured by species diversity [1,2,3,4,5,6,7]
Circumstances allowing for testing the impact of catastrophes on any aspect of ecosystem and evolutionary dynamics are highly unusual due to the longitudinal nature of the work required combined with serendipitous timing
Artesian springs and our study site An archetypal artesian spring is comprised of three parts: a shallow vent or pool where artesian water first reaches the surface, an outflow tail of shallow water and wetland vegetation which grows around the pool and tail and where the substrate allows successive layers of carbonate

Summary

Introduction

Despite the immediate and seemingly far reaching devastation that follows intense natural disturbances, there is an extensive literature showing that such events can generate environmental conditions favourable to the survival, growth and diversification of living organisms and ecosystems, at least as measured by species diversity [1,2,3,4,5,6,7]. Studies have shown parallel responses to disturbance between species and genetic diversity with variation between-sites (beta diversity) increasing and within-sites (alpha diversity) decreasing [8,9,10]. Within species the impact of catastrophes which result in severe reductions in population sizes are neither predicted nor known to result in the promotion of genetic diversity. Circumstances allowing for testing the impact of catastrophes on any aspect of ecosystem and evolutionary dynamics are highly unusual due to the longitudinal nature of the work required combined with serendipitous timing. Having the complementary longitudinal genetic datasets to directly test population genetic consequences of natural disasters is even more exceptional

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