Recombination and loss of complementation: a more than two-fold cost for parthenogenesis

Certain types of asexual reproduction lead to loss of complementation, that is unmasking of recessive deleterious alleles. A theoretical measure of this loss is calculated for apomixis, automixis and endomitosis in the cases of diploidy and polyploidy. The effect of the consequent unmasking of deleterious recessive mutations on fitness is also calculated. Results show that, depending on the number of lethal equivalents and on the frequency of recombination, the cost produced by loss of complementation after few generations of asexual reproduction may be greater than the two-fold cost of meiosis. Maintaining complementation may, therefore, provide a general short-term advantage for sexual reproduction. Apomixis can replace sexual reproduction under a wide range of parameters only if it is associated with triploidy or tetraploidy, which is consistent with our knowledge of the distribution of apomixis.     

Successive virgin births of viable male progeny in the checkered gartersnake,Thamnophis marcianus

In recent years genotyping analysis using mini‐ and microsatellite markers has provided robust DNA‐based support for facultative parthenogenesis (FP) in several lineages of squamate reptiles (snakes and lizards) and sharks. Rather than incidental cases of reproductive error, there is growing evidence that FP is an alternative reproductive strategy and an important mode of reproduction in these phylogenetically divergent vertebrate groups. Because documentation of FP in vertebrates is in its infancy, additional instances supported by molecular genetic methods provide insights that advance our general understanding of this phenomenon. Here, in a female checkered gartersnake (Thamnophis marcianus) reared in isolation since a juvenile, we describe five successive parthenogenetic litters produced over a 7‐year period that resulted in several viable male progeny. Cross species microsatellite amplification was performed across 30 primer pairs derived from Thamnophis spp. and related natricines to the female and nine available progeny. Five loci proved heterozygous in the maternal sample with the progeny differentially homozygous at all but one locus. Combined with evidence pertaining to captive history and litter characteristics, our analysis supports a specific type of FP, terminal fusion automictic parthenogenesis, over the competing hypothesis of long‐term sperm storage. Importantly, we document that a single individual was capable of producing successive litters composed of live parthenogens. In two cases, males achieved adulthood and showed the anatomical potential to demonstrate reproductive competence (normal looking hemipenes and testes). © 2012 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 107 , 566–572.     

Consecutive parthenogenetic births in a spotted eagle ray Aetobatus narinari

Genetic evidence is given to support consecutive parthenogenesis in a spotted eagle ray Aetobatus narinari using nuclear microsatellite genotyping. To date, only a handful of births involving the parthenogenesis process in chondrichthyans have been verified using microsatellite markers and even fewer verified as recurring births. This appears to be the first documented case of this process occurring in a myliobatid species.     

Origin and maintenance of sex: the evolutionary joys of self sex

Sex is generally thought of as meiosis, conjugation, and syngamy, with the primary function of sex believed to be genetic mixing. However, conjugation does not occur with complete automixis, whereas syngamy does not occur with restitutional automixis. Self sex in the forms of automixis and autogamy does not include genetic mixing. Yet sex, including self sex, is necessary for most eukaryotic lineages. What is the purpose of sex without genetic mixing? Obligate self sex is not an evolutionary dead end, but holds the key to understanding the evolutionary origin, function, maintenance, and ubiquity of sex. We extend the rejuvenescence hypothesis that sex provides a necessary developmental reset for multicellular eukaryotes and even many unicellular eukaryotes. Sex reduces additive genetic variance of epigenetic signals, especially cytosine methylation, and of ploidy levels. Furthermore, we argue that syngamy is a modified form of meiosis that maintains ploidy and resets epigenetic signals. Epigenetic resetting is consistent with sex being induced by starvation or desiccation. Diminution of additive genetic variance is consistent with the origin and maintenance of an adaptive trait, sex, that has been present for approximately two billion years. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 98 , 707–728.     

Size Variation of the Nonrecombining Region on the Mating-Type Chromosomes in the Fungal Podospora anserina Species Complex

Sex chromosomes often carry large nonrecombining regions that can extend progressively over time, generating evolutionary strata of sequence divergence. However, some sex chromosomes display an incomplete suppression of recombination. Large genomic regions without recombination and evolutionary strata have also been documented around fungal mating-type loci, but have been studied in only a few fungal systems. In the model fungus Podospora anserina (Ascomycota, Sordariomycetes), the reference S strain lacks recombination across a 0.8-Mb region around the mating-type locus. The lack of recombination in this region ensures that nuclei of opposite mating types are packaged into a single ascospore (pseudohomothallic lifecycle). We found evidence for a lack of recombination around the mating-type locus in the genomes of ten P. anserina strains and six closely related pseudohomothallic Podospora species. Importantly, the size of the nonrecombining region differed between strains and species, as indicated by the heterozygosity levels around the mating-type locus and experimental selfing. The nonrecombining region is probably labile and polymorphic, differing in size and precise location within and between species, resulting in occasional, but infrequent, recombination at a given base pair. This view is also supported by the low divergence between mating types, and the lack of strong linkage disequilibrium, chromosomal rearrangements, transspecific polymorphism and genomic degeneration. We found a pattern suggestive of evolutionary strata in P. pseudocomata. The observed heterozygosity levels indicate low but nonnull outcrossing rates in nature in these pseudohomothallic fungi. This study adds to our understanding of mating-type chromosome evolution and its relationship to mating systems.     

The emerging phylogenetic pattern of parthenogenesis in snakes

Parthenogenesis occurs across a variety of vertebrate taxa. Within squamate reptiles (lizards and snakes), a group for which the largest number of cases has been documented, both obligate and facultative types of parthenogenesis exists, although the obligate form in snakes appears to be restricted to a single basal species of blind snake, Indotyphlops braminus. By contrast, a number of snake species that otherwise reproduce sexually have been found capable of facultative parthenogenesis. Because the original documentation of this phenomenon was restricted to subjects held in captivity and isolated from males, facultative parthenogenesis was attributed as a captive syndrome. However, its recent discovery in nature shifts the paradigm and identifies this form of reproduction as a potentially important feature of vertebrate evolution. In light of the growing number of documented cases of parthenogenesis, it is now possible to review the phylogenetic distribution in snakes and thus identify subtle variations and commonalities that may exist through the characterization of its emerging properties. Based on our findings, we propose partitioning facultative parthenogenesis in snakes into two categories, type A and type B, based on the sex of the progeny produced, their viability, sex chromosome morphology, and ploidy, as well as their phylogenetic position. Furthermore, we introduce a hypothesis (directionality of heterogamety hypothesis) to explain the production of female‐only parthenogens in basal alethinophidian snakes and male‐only parthenogens in caenophidian (advanced) snakes.     

The evolution of meiotic sex and its alternatives

Meiosis is an ancestral, highly conserved process in eukaryotic life cycles, and for all eukaryotes the shared component of sexual reproduction. The benefits and functions of meiosis, however, are still under discussion, especially considering the costs of meiotic sex. To get a novel view on this old problem, we filter out the most conserved elements of meiosis itself by reviewing the various modifications and alterations of modes of reproduction. Our rationale is that the indispensable steps of meiosis for viability of offspring would be maintained by strong selection, while dispensable steps would be variable. We review evolutionary origin and processes in normal meiosis, restitutional meiosis, polyploidization and the alterations of meiosis in forms of uniparental reproduction (apomixis, apomictic parthenogenesis, automixis, selfing) with a focus on plants and animals. This overview suggests that homologue pairing, double-strand break formation and homologous recombinational repair at prophase I are the least dispensable elements, and they are more likely optimized for repair of oxidative DNA damage rather than for recombination. Segregation, ploidy reduction and also a biparental genome contribution can be skipped for many generations. The evidence supports the theory that the primary function of meiosis is DNA restoration rather than recombination.     

Parthenogenesis in a Brazilian Rainbow Boa (Epicrates cenchria cenchria)

A 22‐year‐old captive Brazilian rainbow boa (Epicrates cenchria cenchria) gave birth to four offspring after being housed with a vasectomized male. Sexual reproduction as a result of failed prior vasectomy, recanalization of the vas deferens, or prolonged sperm storage was ruled out using the clinical history, histopathology, and gross necropsy. Short tandem repeat (STR) DNA markers were genotyped in the male, female, and four offspring. None of the offspring possessed a diagnostic STR allele present in the potential sire. In addition, all offspring were homozygous at each STR locus evaluated, supporting parthenogenetic reproduction. This is the first report of parthenogenesis in a Brazilian rainbow boa and has implications for the conservation of reptiles maintained in captive breeding programs. Zoo Biol. 32:172–176, 2013. © 2012 Wiley Periodicals, Inc.     

Molecular genetic evidence for alternative reproductive strategies in North American pitvipers (Serpentes: Viperidae): long‐term sperm storage and facultative parthenogenesis

The first documentation of facultative parthenogenesis (FP) in non‐avian reptiles (snakes) occurred in 1997, following the application of molecular genetic methods for parentage analysis, and since has been described in only four additional snake species. Here, in two species of live‐bearing (viviparous) North American pitviper snakes, using microsatellite DNA fingerprinting, we describe the first record of a virgin birth by FP in the copperhead (Agkistrodon contortrix), and the first genetically confirmed case of long‐term sperm storage (LTSS) of exceptional duration (5 years) in the eastern diamond‐backed rattlesnake (Crotalus adamanteus). The capacity of female squamate reptiles (snakes, lizards, and amphisbaenians) to store viable sperm for extended periods of time is a competing hypothesis to FP, and it is often inferred when interpreting certain births where adult females have been isolated from adult male mates for prolonged periods. On reviewing the literature of certain cases of LTSS in snakes, we provide compelling support for the prevalence of FP, casting doubt over the widespread acceptance of LTSS. Accordingly, with the discovery of FP in squamates and the results of the present study, we advocate that in order to differentiate between LTSS and FP, especially under natural conditions, rigorous molecular testing will be required. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 104 , 934–942.     

Parthenogenesis in a large‐bodied requiem shark,the blacktip Carcharhinus limbatus

Genetic evidence is provided for parthenogenesis in a large‐bodied shark, the blacktip Carcharhinus limbatus, from the speciose and commercially important family Carcharhinidae, the first verified case of asexual development in this lineage and only the second for any chondrichthyan. The parthenogenetic embryo exhibited elevated homozygosity relative to its mother, indicating that automictic parthenogenesis is the most likely mechanism. Although this finding shows that parthenogenesis is more common and widespread in sharks than previously realized and supports the early existence of parthenogenetic abilities in vertebrates, the adaptive significance of automixis in these ancient fishes remains unclear.