Rare gene capture in predominantly androgenetic species

Abstract

The long-term persistence of completely asexual species is unexpected. Although asexuality has short-term evolutionary advantages, a lack of genetic recombination leads to the accumulation over time of deleterious mutations. The loss of individual fitness as a result of accumulated deleterious mutations is expected to lead to reduced population fitness and possible lineage extinction. Persistent lineages of asexual, all-female clones (parthenogenetic and gynogenetic species) avoid the negative effects of asexual reproduction through the production of rare males, or otherwise exhibit some degree of genetic recombination. Another form of asexuality, known as androgenesis, results in offspring that are clones of the male parent. Several species of the Asian clam genus Corbicula reproduce via androgenesis. We compared gene trees of mitochondrial and nuclear loci from multiple sexual and androgenetic species across the global distribution of Corbicula to test the hypothesis of long-term clonality of the androgenetic species. Our results indicate that low levels of genetic capture of maternal nuclear DNA from other species occur within otherwise androgenetic lineages of Corbicula. The rare capture of genetic material from other species may allow androgenetic lineages of Corbicula to mitigate the effects of deleterious mutation accumulation and increase potentially adaptive variation. Models comparing the relative advantages and disadvantages of sexual and asexual reproduction should consider the possibility of rare genetic recombination, because such events seem to be nearly ubiquitous among otherwise asexual species.

Fig. 1.

Maximum likelihood gene tree estimate of the third intron of the nuclear α-amylase gene. Numbers above the branch are Bayesian posterior probabilities, and numbers below are likelihood bootstrap proportions. Species are labeled as putatively sexual or asexual on the basis of morphology and/or lack of population-level genetic variation (Table S2). Two individuals were sequenced for C. sp. B and C. loehensis; these are distinguished by number following the species name.

Fig. 2.

Maximum likelihood gene tree estimate of a putative nuclear intron of the α subunit of adenosine triphosphate synthase. Numbers above the branch are Bayesian posterior probabilities, and numbers below are likelihood bootstrap proportions. Species are labeled as sexual or asexual on the basis of morphology and lack of population-level genetic variation (Table S2).

Fig. 3.

Expected relationships between mitochondrial and nuclear markers in androgenetic Corbicula, given four possible scenarios. Central lines between trees indicate where taxa in the mitochondrial tree are found on the nuclear tree. Androgenetic Corbicula are in red and referred to by letter for ease of comparison. A: C. sp. A (North America, The Netherlands); B: C. sp. B (North America); C: C. sp. C (South America, The Netherlands); D: C. fluminea (Korea, Thailand); E: C. fluminea (Taiwan); F: C. fluminea (Philippines). (A) Multiple origins or single origin at * and reversion; (B) single origin with mitochondrial capture; (C) single origin with mitochondrial and nuclear capture at ^; (D) two origins at * with mitochondrial capture.

Fig. 4.

Observed relationships between mitochondrial and nuclear markers in androgenetic Corbicula. Central lines between trees indicate where taxa in the mitochondrial tree are found on the nuclear tree. Androgenetic Corbicula are in red and referred to by letter for ease of comparison. A: C. sp. A (North America, The Netherlands); B: C. sp. B (North America); C: C. sp. C (South America, The Netherlands); D: C. fluminea (Korea, Thailand); E: C. fluminea (Taiwan); F: C. fluminea (Philippines). (A) Comparison between the mitochondrial cox-I tree from Hedtke et al. (15) and the nuclear amy tree. (B) Comparison between the mitochondrial cox-I tree and the nuclear atps-α tree.