Evolutionary origin and phylogeography of the diploid obligate parthenogen Artemia parthenogenetica (Branchiopoda: Anostraca).

Joaquín Muñoz,Andy J Green,Francisco Amat,Ciro Rico,Jordi Figuerola,Africa Gómez

doi:10.1371/journal.pone.0011932

Abstract

BackgroundUnderstanding the evolutionary origin and the phylogeographic patterns of asexual taxa can shed light on the origin and maintenance of sexual reproduction. We assessed the geographic origin, genetic diversity, and phylogeographic history of obligate parthenogen diploid Artemia parthenogenetica populations, a widespread halophilic crustacean.Methodology/Principal FindingsWe analysed a partial sequence of the Cytochrome c Oxidase Subunit I mitochondrial gene from an extensive set of localities (including Eurasia, Africa, and Australia), and examined their phylogeographic patterns and the phylogenetic relationships of diploid A. parthenogenetica and its closest sexual relatives. Populations displayed an extremely low level of mitochondrial genetic diversity, with one widespread haplotype shared by over 79% of individuals analysed. Phylogenetic and phylogeographic analyses indicated a multiple and recent evolutionary origin of diploid A. parthenogenetica, and strongly suggested that the geographic origin of parthenogenesis in Artemia was in Central Asia. Our results indicate that the maternal sexual ancestors of diploid A. parthenogenetica were an undescribed species from Kazakhstan and A. urmiana.Conclusions/SignificanceWe found evidence for multiple origin of parthenogenesis in Central Asia. Our results indicated that, shortly after its origin, diploid A. parthenogenetica populations underwent a rapid range expansion from Central Asia towards the Mediterranean region, and probably to the rest of its current geographic distribution. This contrasts with the restricted geographic distribution, strong genetic structure, and regional endemism of sexual Artemia lineages and other passively dispersed sexual continental aquatic invertebrates. We hypothesize that diploid parthenogens might have reached their current distribution in historical times, with a range expansion possibly facilitated by an increased availability of suitable habitat provided by anthropogenic activities, such as the spread of solar saltworks, aided by their natural dispersal vectors (i.e., waterbirds).

Highlights

Parthenogenetic organisms tend to have broadly distributed genetic lineages, wider geographic distributions than their sexual relatives, and a propensity to occur in marginal areas
Genetic diversity and haplotype distribution COI sequences (658 bp) from 102 individuals collapsed into a total of eight haplotypes from the 12 A. parthenogenetica populations analysed
Our results show that diploid Artemia parthenogenetica has an extremely low level of mtDNA diversity across most of its known distribution range

Summary

Introduction

Parthenogenetic organisms tend to have broadly distributed genetic lineages, wider geographic distributions than their sexual relatives, and a propensity to occur in marginal areas (see [1] and references therein). Several non-exclusive hypotheses have been put forward to explain this phenomenon, ranging from their better colonisation abilities through reproductive assurance (i.e. a single female individual can reproduce and establish a new population) to their hybrid origin, polyploidy, or metapopulation dynamics (see [2] for a detailed discussion) Some of these hypotheses involve non-equilibrium scenarios for the advantage of parthenogenetic strategies (e.g. habitat dynamics or climatic trends could temporally favour parthenogenetic strategies). Examples of wide geographic distribution of genetic lineages have been reported in a few species with mixed or alternative reproduction modes, including hermaphroditism, which, like obligate parthenogens, can potentially establish populations from a single propagule (i.e. diapausing egg) [15,19,20] In all these cases, the historical availability of suitable habitat, either through human-mediated inoculations or postglacial processes, seems to have favoured organisms with unisexual modes of reproduction. We assessed the geographic origin, genetic diversity, and phylogeographic history of obligate parthenogen diploid Artemia parthenogenetica populations, a widespread halophilic crustacean

Methods

Results

Conclusion