Abstract

The extreme rarity of asexual vertebrates in nature is generally explained by genomic decay due to absence of meiotic recombination, thus leading to extinction of such lineages. We explore features of a vertebrate asexual genome, the Amazon molly, Poecilia formosa, and find few signs of genetic degeneration but unique genetic variability and ongoing evolution. We uncovered a substantial clonal polymorphism and, as a conserved feature from its interspecific hybrid origin, a 10-fold higher heterozygosity than in the sexual parental species. These characteristics seem to be a principal reason for the unpredicted fitness of this asexual vertebrate. Our data suggest that asexual vertebrate lineages are scarce not because they are at a disadvantage, but because the genomic combinations required to bypass meiosis and to make up a functioning hybrid genome are rarely met in nature.

Highlights

  • Asexual lineages present a paradox to biology

  • The classical model of demise, Muller’s ratchet[1,2], states that deleterious mutations cannot be purged without meiosis, and their accumulation will lead to genomic decay and eventually extinction[3,4]

  • The number of proteincoding genes for each was similar to P. formosa: 25,220 for P. latipinna and 25,341 for P. mexicana

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Summary

Introduction

Asexual lineages present a paradox to biology. Overwhelmingly, theory predicts that asexual reproduction would have several main disadvantages. All theories agree that the disadvantages of asexual propagation quickly outweigh this advantage, and that clonality should eventually lead to extinction[3,9] Mixed support for this prediction exists: some asexual species, for example, the obligate asexual waterflea, show deleterious mutation accumulation and are evolutionary extremely short-lived[10], other asexuals are older than predicted and successful colonizers in their natural habitats[11,12,13,14]. P. formosa became one of the paradigmatic cases that appear to violate the age predictions of Muller’s ratchet and the dynamics of the Red Queen hypothesis It is a highly successful colonizer of diverse habitats over a wide geographical range and mitochondrial DNA-based estimates postulated a much longer existence, exceeding the theoretical extinction time[10,12,14]. In this study we investigate the ancestral history of the P. formosa genome and reveal its novel features

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