Mating-Induced Trade-Offs upon Egg Production versus Fertilization and Offspring’s Survival in a Sawfly with Facultative Parthenogenesis

Investigation of mating-induced trade-offs between reproduction and survival is conducive to provide evolutionary insights into reproductive strategies and aging. Here, we used RNAseq and bioinformatics to reveal mating-induced changes of genes and pathways related to reproduction and survival in female Cephalcia chuxiongica, a pine defoliator with facultative parthenogenesis and long larval dormancy. Results showed that mating induced substantial downregulation on genes and pathways associated to immunity, stress response, and longevity. However, mating induced divergent reproductive response, with downregulation on genes and pathways related to egg production while upregulation on genes and pathways related to egg fertilization. Considering the nature of limited resources in adults, low fecundity, and egg protection behavior in C. chuxiongica, we suggest that mating triggers trade-offs between reproduction and survival in this insect and females of this species may have evolved specific strategies to adapt to the environmental and hosts’ conditions, e.g., restrict whole fecundity to ensure higher fertilization and offspring’s survival. Moreover, mating induced significant responses on genes and pathways that play important roles in vertebrate reproduction while their function in insects are unclear, such as the progesterone-mediated oocyte maturation pathway; the significant regulation after mating suggests that their function may be evolutionarily conserved in animal kingdom.

Fisher vs. The Worms: Extraordinary Sex Ratios in Nematodes and the Mechanisms That Produce Them

Parker, Baker, and Smith provided the first robust theory explaining why anisogamy evolves in parallel in multicellular organisms. Anisogamy sets the stage for the emergence of separate sexes, and for another phenomenon with which Parker is associated: sperm competition. In outcrossing taxa with separate sexes, Fisher proposed that the sex ratio will tend towards unity in large, randomly mating populations due to a fitness advantage that accrues in individuals of the rarer sex. This creates a vast excess of sperm over that required to fertilize all available eggs, and intense competition as a result. However, small, inbred populations can experience selection for skewed sex ratios. This is widely appreciated in haplodiploid organisms, in which females can control the sex ratio behaviorally. In this review, we discuss recent research in nematodes that has characterized the mechanisms underlying highly skewed sex ratios in fully diploid systems. These include self-fertile hermaphroditism and the adaptive elimination of sperm competition factors, facultative parthenogenesis, non-Mendelian meiotic oddities involving the sex chromosomes, and environmental sex determination. By connecting sex ratio evolution and sperm biology in surprising ways, these phenomena link two “seminal” contributions of G. A. Parker.

Exceptional long-term sperm storage by a female vertebrate

Females of many vertebrate species have the capacity to store sperm within their reproductive tracts for prolonged periods of time. Termed long-term sperm storage, this phenomenon has many important physiological, ecological, and evolutionary implications, particularly to the study of mating systems, including male reproductive success and post-copulatory sexual selection. Reptiles appear particularly predisposed to long-term sperm storage, with records in most major lineages, with a strong emphasis on turtles and squamates (lizards, snakes, but not the amphisbaenians). Because facultative parthenogenesis is a competing hypothesis to explain the production of offspring after prolonged separation from males, the identification of paternal alleles through genetic analysis is essential. However, few studies in snakes have undertaken this. Here, we report on a wild-collected female Western Diamond-backed Rattlesnake, Crotalus atrox, maintained in isolation from the time of capture in September 1999, that produced two healthy litters approximately one and six years post capture. Genetic analysis of the 2005 litter, identified paternal contribution in all offspring, thus rejecting facultative parthenogenesis. We conclude that the duration of long-term sperm storage was approximately 6 years (71 months), making this the longest period over which a female vertebrate has been shown to store sperm that resulted in the production of healthy offspring.

Genome-wide data implicate terminal fusion automixis in king cobra facultative parthenogenesis

Facultative parthenogenesis (FP) is widespread in the animal kingdom. In vertebrates it was first described in poultry nearly 70 years ago, and since then reports involving other taxa have increased considerably. In the last two decades, numerous reports of FP have emerged in elasmobranch fishes and squamate reptiles (lizards and snakes), including documentation in wild populations of both clades. When considered in concert with recent evidence of reproductive competence, the accumulating data suggest that the significance of FP in vertebrate evolution has been largely underestimated. Several fundamental questions regarding developmental mechanisms, nonetheless, remain unanswered. Specifically, what is the type of automixis that underlies the production of progeny and how does this impact the genomic diversity of the resulting parthenogens? Here, we addressed these questions through the application of next-generation sequencing to investigate a suspected case of parthenogenesis in a king cobra (Ophiophagus hannah). Our results provide the first evidence of FP in this species, and provide novel evidence that rejects gametic duplication and supports terminal fusion as a mechanism underlying parthenogenesis in snakes. Moreover, we precisely estimated heterozygosity in parthenogenetic offspring and found appreciable retained genetic diversity that suggests that FP in vertebrates has underappreciated evolutionary significance.

Facultative Parthenogenesis in a Diamondback Water Snake (Nerodia rhombifer)

Here we describe a case of facultative parthenogenesis in a diamondback water snake (Nerodia rhombifer). An adult female N. rhombifer kept in captivity produced four unfertilized ova, one stillborn and one live neonate in July 2016. The neonates had characteristic abnormalities in morphology and were determined as males, suggestive of a parthenogenetic event. Stillborn and live neonates along with the mother and four unrelated N. rhombifer were genetically screened at twelve microsatellite loci. Results confirmed that the reproductive event represented a case of facultative parthenogenesis. In light of previous reports of facultative parthenogenesis in the genera Nerodia and Thamnophis, these results suggest that this reproductive mode may be a widespread phenomenon in the Natricinae as a whole.

Evidence of facultative parthenogenesis in three Neotropical pitviper species of the Bothrops atrox group

We examined four suspected cases of facultative parthenogenesis in three species of a neotropical lineage of pitvipers of the Bothrops atrox group. Reproduction without mating was observed in captive females of B. atrox, B. moojeni and B. leucurus housed alone for seven years (the two former species) and nine years (the latter one). In addition to the observation of captivity data, we investigated molecularly this phenomenon using heterologous microsatellites. DNA was extracted from the mothers’ scales or liver, from embryo and newborn fragments, and yolked ova. Four of the microsatellites showed good amplification using Polymerase Chain Reaction and informative band segregation patterns among each mother and respective offspring. Captivity information, litter characteristics (comparison of the number of newborns, embryos and yolked ova) and molecular data altogether agreed with facultative parthenogenesis predictions in at least three out of the four mothers studied: B. atrox (ID#933) was heterozygous for three out of the four markers, and the sons S1 and S2 were homozygous; B. moojeni (BUT86) was heterozygous for two out of four markers, offspring S1, S3, E2, and E4, and O1 to O6 were homozygous; and B. leucurus (MJJS503) was heterozygous for three out of four markers, and son E1 and O1 were homozygous. B. moojeni (BUT44) was homozygous for all loci analyzed in the mother and offspring, which although not informative is also consistent with parthenogenesis. This study represents the first molecular confirmation of different pitviper species undergoing facultative parthenogenesis among Neotropical endemic snakes.

Extremely Widespread Parthenogenesis and a Trade-Off Between Alternative Forms of Reproduction in Mayflies (Ephemeroptera)

Studying alternative forms of reproduction in natural populations is of fundamental importance for understanding the costs and benefits of sex. Mayflies are one of the few animal groups where sexual reproduction co-occurs with different types of parthenogenesis, providing ideal conditions for identifying benefits of sex in natural populations. Here, we establish a catalog of all known mayfly species capable of reproducing by parthenogenesis, as well as species unable to do so. Overall, 1.8% of the described species reproduce parthenogenetically, which is an order of magnitude higher than reported in other animal groups. This frequency even reaches 47.8% if estimates are based on the number of studied rather than described mayfly species, as reproductive modes have thus far been studied in only 17 out of 42 families. We find that sex is a more successful strategy than parthenogenesis (associated with a higher hatching success of eggs), with a trade-off between the hatching success of parthenogenetic and sexual eggs. This means that improving the capacity for parthenogenesis may come at a cost for sexual reproduction. Such a trade-off can help explain why facultative parthenogenesis is extremely rare among animals despite its potential to combine the benefits of sexual and parthenogenetic reproduction. We argue that parthenogenesis is frequently selected in mayflies in spite of this probable trade-off because their typically low dispersal ability and short and fragile adult life may frequently generate situations of mate limitation in females. Mayflies are currently clearly underappreciated for understanding the benefits of sex under natural conditions.

Extremely widespread parthenogenesis and a trade-off between alternative forms of reproduction in mayflies (Ephemeroptera)

Studying alternative forms of reproduction in natural populations is of fundamental importance for understanding the costs and benefits of sex. Mayflies are one of the few animal groups where sexual reproduction co-occurs with different types of parthenogenesis, providing ideal conditions for identifying benefits of sex in natural populations. Here, we establish a catalogue of all known mayfly species capable of reproducing by parthenogenesis, as well as mayfly species unable to do so. Overall, 1.8% of the described species reproduce parthenogenetically, which is an order of magnitude higher than reported in other animal groups. This frequency even reaches 47.8% if estimates are based on the number of studied rather than described mayfly species. In terms of egg-hatching success, sex is a more successful strategy than parthenogenesis, and we found a trade-off between the efficiency of sexual and parthenogenetic reproduction across species. This means that improving the capacity for parthenogenesis may come at the cost of being less able to reproduce sexually, even in facultative parthenogens. Such a trade-off can help explain why facultative parthenogenesis is extremely rare among animals despite its potential to combine the benefits of sexual and parthenogenetic reproduction. We argue that parthenogenesis is frequently selected in mayflies in spite of this probable trade-off because their typically low dispersal ability and short and fragile adult life may frequently generate situations of mate limitation in females. Mayflies are currently clearly underappreciated for understanding the benefits of sex under natural conditions.