Most animals have female and male genders. Considering the investment of energy required for sexual reproduction, it is interesting to know why this strategy has been conserved during evolution in some species. The effort that goes into mating result in less reproduction. Moreover, meiotic recombination entails important inherent risks in terms of genomic instability, and the creation/production of separate sex, with specific genetic and physiological features distinct from the female, may be regarded as a burden for the evolutionary success of the species. On the contrary, self-fertilizing animals tend to be less genetically diverse and this makes them more unprotected against harmful mutations that can drive them to extinction or even more vulnerable to unpredictable threats such as parasites. The reasons indicated above have made the scientific community consider that the production of males in a species is of great value (1).
Today, up to 30% of all animal species are known to be hermaphrodites instead of females. These hermaphrodites have a low rate of mating to maintain some of the advantages of sex. A rarer and more extreme strategy in the animal world is abandoning sex completely, which is the case for some parthenogenetic animals (2).
This kind of animals has a special type of asexual reproduction in which the ‘female’ uses the sperm of males in order to activate their oocytes, strategy known as gynogenesis. In this case, the DNA of male’s sperm is not used and only female individuals are produced. For instance, Mesorhabditis belari uses this strategy. However, it has been observed that it is unable to reproduce without the males of its species (3).
Grosmaire et al. found during their research that M. belari produced two kinds of embryos: gynogenetic embryos that would give rise to females, the most common ones, and amphimictic embryos, which would grow as males (Fig.1A) (3). After fertilization, female meiosis restarted and a single division occurs resulting in one polar body and a female pronucleus with 20 chromosomes. As for the male DNA, it condenses, suggesting that it is not passed on to the progeny, despite the strong asters formed by the sperm centrosomes that make contact with the female genetic material on its way to form the first mitotic spindle. In this case, the two meiotic divisions were observed, obtaining two polar bodies and a female pronucleus with 10 chromosomes (Fig. 1B). Despite the differences, both embryos were diploid. After this experiment, the number of males and females among the progeny were counted (Fig. 1C). In addition, single nucleotide polymorphism (SNP) genotyping confirmed that only the males were the result of true fertilization (3).
To explain why they only recovered males from amphimictic embryos, the authors decided to sequence and compare male to female genomes, being able to identify certain male-specific genes. Such findings suggested the existence of a Y chromosome. Additionally, they found genes that were two times more expressed in females. By genotyping specific SNPs located in these female contigs they confirmed that males only presented one maternal allele, in line with X-linked segregation.
Therefore, the authors concluded that sex determination in M. belari is based on the XX/XY system (see supplemental Table 3 and Figure 2 from the original paper) (3).
To determine when Y bias happened, DNA was labeled with a Y-specific probe and analyzed by fluorescence in situ hybridization (FISH). In both, male gonad and female spermatheca, 50% of sperm nuclei were detected to be positive for this label. This finding suggests that male sperm were carrying X as well as Y chromosomes, which would be transferred to the embryos. In addition, Y fluorescence was detected in 66 out of 76 gynogenetic embryos (Fig. 2B). This indicates that 90% of the gynogenetic embryos would be fertilized by Y-bearing spermatozoa in M. belari, and 10% of the embryos would be fertilized by an X-bearing sperm. This low proportion of gynogenetic embryos produced by X-bearing spermatozoa points to a small percentage (<1%) of XX amphimictic eggs that are produced but do not progress to the adult stage. These findings are in accordance to previous data and might be explained due to the low capacity of X-bearing sperm to penetrate into the oocyte and to the low developmental potential of those amphimictic eggs so fertilized (3).
Since the gynogenetic embryos exclude paternal DNA, the same situation was the focus of interest on amphimictic embryos in this paper. The authors asked whether the males preferentially transmitted their alleles to their sons by excluding female genes. To test this, four independent SNPs were studied in the autosomes. Based on segregation ratios, the female genome was found to be eventually combined with the male genome, with the exception of the Y chromosome, since the paternal genome would be diluted with the mother’s genome in each generation (3).
Another interesting question was the proportion of males produced in M. belari. Females only produce males if these mate with their sibling females; otherwise, male production is not efficient. In this context, the authors wondered what proportion of males should be produced to reach the maximum efficiency in the mating process without fertilizing unrelated females. A game theory model was proposed to investigate the evolutionary stable strategy (ESS) of sex ratio (Fig.3). In this study, ESS was dependent on two variables including sperm availability and patch size. Finally, they observed a slight increase of ESS with a defined dispersion rate and with a particular limitation in the sperm number (3).
Male production in M. belari is an interesting strategy that may avoid the competition for males of other species by creating an efficient number of them. Moreover, since Y-bearing sperm is much more competent than X-bearing sperm, it is tempting to think that creation of gynogenesis is a strategy that reduces this advantage in a parthenogenetic species such as M. belari (3).
Now it is your turn. What do you think? Would you consider gynogenesis as a way to decrease the advantage of Y-bearing sperm? Would you like more content like this? Let us know in the comments!
- Schwarz EM. Evolution: A Parthenogenetic Nematode Shows How Animals Become Sexless. Curr Biol CB. 2017 Oct 9;27(19):R1064–6.
- van der Kooi CJ, Schwander T. Parthenogenesis: Birth of a New Lineage or Reproductive Accident? Curr Biol. 2015 Aug 3;25(15):R659–61.
- Grosmaire M, Launay C, Siegwald M, Brugière T, Estrada-Virrueta L, Berger D, et al. Males as somatic investment in a parthenogenetic nematode. Science. 2019 Mar 15;363(6432):1210–3.