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Rare Gene Capture in Predominantly Androgenetic Species

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Rare Gene Capture in Predominantly Androgenetic Species Rare gene capture in predominantly androgenetic species Shannon M. Hedtkea,1, Matthias Glaubrechtb, and David M. Hillisa,1 aSection of Integrative Biology and Center for Computational Biology and Bioinformatics, University of Texas at Austin, Austin, TX 78712; and bMuseum für Naturkunde Berlin, Leibniz Institute for Research in Evolution and Biodiversity at the Humbolt University Berlin, D-10115 Berlin, Germany Contributed by David M. Hillis, April 27, 2011 (sent for review February 28, 2011) The long-term persistence of completely asexual species is un- the persistence of androgenetic species, and thus the time expected. Although asexuality has short-term evolutionary advan- available to generate asexual diversity? Or is the observed di- tages, a lack of genetic recombination leads to the accumulation versity a result of recent, replicate origins [as in ostracods, stick over time of deleterious mutations. The loss of individual fitness as insects, and water fleas (17–19)]? a result of accumulated deleterious mutations is expected to lead Many asexual lineages have mechanisms for rare genetic cap- to reduced population fitness and possible lineage extinction. ture (20–24). In parthenogenetic lineages, a male may be pro- Persistent lineages of asexual, all-female clones (parthenogenetic duced after several generations of female clonal reproduction, and gynogenetic species) avoid the negative effects of asexual and sex could occur between the parthenogens and the rare male reproduction through the production of rare males, or otherwise (25). In several pathogenic fungi that seem to be asexual, DNA exhibit some degree of genetic recombination. Another form of sequencing revealed the presence of functional genes for mating asexuality, known as androgenesis, results in offspring that are and meiosis, suggesting that cryptic or unobserved sex could be clones of the male parent. Several species of the Asian clam genus occurring (26). In one type of asexual reproduction, gynogenesis, Corbicula reproduce via androgenesis. We compared gene trees of females require sperm from males of closely related sexual mitochondrial and nuclear loci from multiple sexual and androge- species to activate embryogenesis, but males do not regularly netic species across the global distribution of Corbicula to test the contribute genes to offspring. For example, even though behav- hypothesis of long-term clonality of the androgenetic species. Our iors associated with sexual reproduction are inherited from results indicate that low levels of genetic capture of maternal nu- a sexual ancestor, Amazon mollies (Poecilia formosa) are con- clear DNA from other species occur within otherwise androgenetic sidered asexual because daughters are usually genetically iden- lineages of Corbicula. The rare capture of genetic material from tical to their mothers. However, gametic interactions between other species may allow androgenetic lineages of Corbicula to sexuals and asexuals lead to rare genetic capture: micro- mitigate the effects of deleterious mutation accumulation and in- chromosomes are passed on from host males, and these micro- crease potentially adaptive variation. Models comparing the relative chromosomes contain genes with effects on phenotype (27, 28). advantages and disadvantages of sexual and asexual reproduction Some of these microchromosomes are inherited by subsequent should consider the possibility of rare genetic recombination, be- generations of female clones (27, 29). Rarely, entire chromo- cause such events seem to be nearly ubiquitous among otherwise somes of haploid sperm are integrated with the diploid maternal asexual species. genome, causing triploid, gynogenetic offspring (30), although triploidy is unstable and individuals can end up with both diploid Muller’s ratchet | Meselson effect | Hill-Robertson effects | phylogenetics and triploid somatic cells (31). Thus, gynogenetic lineages that gain genetic material from males may persist for longer periods lthough asexual reproduction is widely distributed across of time than otherwise expected (32). Aeukaryotes, obligate asexuality is comparatively rare, and The ancient asexual bdelloid rotifers are often considered an obligately asexual species tend to be of recent origin (1–4). Be- exception to the rule of persistent asexuality. No males have cause of this observed rarity, there are presumably costs to ob- been observed in either contemporary or fossil populations going ligate asexuality that allow sexual lineages to outcompete their back at least 35 million years (33), and genomes of many bdel- asexual relatives, even though sexual reproduction itself carries loids contain highly divergent alleles (34)—some to the point costs [particularly the “two-fold cost of sex”: the cost of pro- where two alleles may have different functions (35). However, ducing males or the cost of meiosis (2, 3)]. The literature on during cycles of desiccation, the genome is fragmented. When genetic (or mutational) costs to asexuality is extensive, but the the rotifer is rehydrated, DNA from the environment may be main ideas can be broadly summarized as (i) asexuals can only incorporated into the genome during chromosome repair, re- rely on mutation to generate adaptive variation (e.g., refs. 1 and sulting in genetic recombination (36). Between morphologically 5); and (ii) deleterious mutations accumulate faster in asexuals and genetically distinct species, some nearly identical alleles are than sexuals (e.g., refs. 6–9). When more than one asexual lin- shared, even though these species seem to have been reproducing asexually for many millions of years (37). eage is observed in a closely related group of organisms, some Corbicula process must either allow for diversification despite the costs, or In androgenetic , genetic recombination could occur else repeatedly generate new asexual lineages. Understanding when gametes interact during reproduction. After fertilization, mechanisms that drive asexual diversity can reveal much about maternal nuclear chromosomes are extruded from the egg cell; the costs and benefits of asexual reproduction. Androgenesis is a form of asexual reproduction in which off- Author contributions: S.M.H. and D.M.H. designed research; S.M.H. and M.G. performed spring are clones of the father (10, 11). Several species of Asian research; S.M.H. analyzed data; and S.M.H. and D.M.H. wrote the paper. clams in the genus Corbicula produce paternal clones through The authors declare no conflict of interest. androgenesis (12–14). Androgenetic Corbicula are hermaphro- Data deposition: The sequences reported in this paper have been deposited in the Gen- dites and fertilize both their own eggs and eggs from closely Bank database (accession nos. JF899599–JF899769). related congeners to make paternal clones that do not incor- 1To whom correspondence may be addressed. E-mail: [email protected] or porate maternal nuclear chromosomes (15, 16). Could the in- [email protected]. Corbicula teraction between gametes of closely related species This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. allow rare sex between lineages, changing our expectations for 1073/pnas.1106742108/-/DCSupplemental. 9520–9524 | PNAS | June 7, 2011 | vol. 108 | no. 23 www.pnas.org/cgi/doi/10.1073/pnas.1106742108 Downloaded by guest on September 23, 2021 only paternal nuclear chromosomes from the sperm remain in .98 C. sp. A (N. Am.) the zygote (12–14). Mitochondria, however, are maternally in- .99 .74 C. sp. C (S. Am.) .70 C. sp. A (N. Am., Netherlands), herited, so offspring possess the maternal mitochondrial genome C. fluminea (Korea, Philippines, Thailand) and the paternal nuclear genome. Phylogenies built from mito- asexual .91 C. fluminea (Thailand, Korea) chondrial vs. nuclear markers can be compared to identify 1.0 .95 C. sp. B (N. Am.) .99 between-species genetic recombination (10). Well-supported C. sp. B (N. Am.) phylogenetic incongruence between mitochondrial and nuclear .99 C. sandai (Japan) sexual gene trees would be a signal of egg-capture (and thus mito- .70 .86 C. sp. B (N. Am.) .99 C. fluminea (Korea) chondrial genome-capture) in the genus (10, 15, 16). Nuclear asexual gene-capture by one (paternal) species would be indicated if C. fluminea (Thailand) nuclear alleles found within a single individual were highly di- C. sp. C (Netherlands) 1.0 vergent and also had different evolutionary histories (as seen 1.0 C. tobiae (Indonesia) .89 .83 C. moltkiana (Indonesia) sexual after sexual hybridization between species). We used these as- C. loehensis (Indonesia) Corbicula .49 sumptions to compare a mitochondrial phylogeny of .53 1.0 C. sp. A (N. Am.) (from ref. 16) to two phylogenies built using single-copy nuclear .96 C. fluminea (Philippines, Taiwan) asexual fi .92 introns. We nd evidence that multiple androgenetic lineages 0.01 C. fluminea (Philippines) .71 have captured mitochondrial and nuclear DNA from other spe- .58 C. fluminea (Philippines) .40 cies and suggest that rare sex could generate genetic diversity and C. matannensis (Indonesia) sexual allow androgenetic lineages to persist for longer than expected. Fig. 2. Maximum likelihood gene tree estimate of a putative nuclear intron of the α subunit of adenosine triphosphate synthase. Numbers above the Results branch are Bayesian posterior probabilities, and numbers below are likelihood We estimated phylogenies for two single-locus nuclear markers: bootstrap proportions. Species are labeled as sexual or asexual on the basis
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