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11 Apr 2023
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Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?

Facultative parthenogenesis and transitions from sexual to asexual reproduction

Recommended by ORCID_LOGO based on reviews by 3 anonymous reviewers

Despite a vast array of ways in which organisms can reproduce (Bell, 1982), most animals engage in sexual reproduction (Otto & Lenormand, 2002). A fascinating alternative to sex is parthenogenesis, where offspring are produced asexually from a gamete, typically the egg, without receiving genetic material from another gamete (Simon, Delmotte, Rispe, & Crease, 2003). One of the long-standing questions in the field is why parthenogenesis is not more widespread, given the costs associated with sex (Otto & Lenormand, 2002).  Natural populations of most species appear to be reproducing either sexually or parthenogenetically, even if a species can employ both reproductive modes (Larose et al 2023). Larose et al (2023) highlight the conundrum in this pattern, as organisms that are capable of employing parthenogenesis facultatively would be able to gain the benefits of both modes of reproduction. Why then, is facultative parthenogenesis not more common?

Larose et al (2023) propose that constraints on being efficient in both sexual and asexual reproduction could cause a trade-off between reproductive modes that favours an obligate strategy of either sex or no sex. This would provide an explanation for why facultative parthenogenesis is rare. Timema stick insects provide an excellent system to investigate reproductive strategies, as some species have parthenogenetic females, while other species are sexual, and they show repeated transitions from sexual reproduction to obligate parthenogenesis (Schwander & Crespi, 2009). The authors performed comprehensive and complementary studies in a recently discovered species T. douglasi, in which populations show both modes of reproduction, with some populations consisting only of females and others showing equal proportions of males and females. The sex ratio varied significantly, with the proportion of females ranging between 43-100% across 29 populations. These populations form a monophyletic clade with clustering into three genetic lineages and only a few cases of admixture. Females from all populations were capable of producing unfertilized eggs, but the hatching success varied hugely among populations and lineages (3-100%). Parthenogenetically produced offspring were homozygous, showing that parthenogenesis causes a complete loss of heterozygosity in a single generation. After producing eggs as virgins, females were mated to assess the capacity to also reproduce sexually, and fertilization increased the hatching success of eggs in two lineages. In one lineage, in which the hatching success of unfertilized eggs is similar to that of other sexually reproducing Timema species, fertilization reduced egg-hatching success, indicating a trade-off between reproductive modes with parthenogenetic reproduction performing best. Approximately 58% of the offspring produced after mating were fertilized, demonstrating the capacity of females to reproduce parthenogenetically also after mating has occurred, however with huge variation among individuals.

This wonderful and meticulously performed study produces strong and complementary evidence for facultative parthenogenesis in T. douglasi populations. The study shows large variation in how reproductive mode is employed, supporting the existence of a trade-off between sexual and parthenogenetic reproduction. This might be an example of an ongoing transition from sexual to asexual reproduction, which indicates that obligate parthenogenesis may derive via transient facultative parthenogenesis. 

REFERENCES

Bell, G. (1982) The Masterpiece of Nature: The Evolution and Genetics of Sexuality. University of California Press. 635 p.

Otto, S. P., & Lenormand, T. (2002). Resolving the paradox of sex and recombination. Nature Reviews Genetics, 3(4), 252-261. https://doi.org/10.1038/nrg761

Schwander, T., & Crespi, B. J. (2009). Multiple direct transitions from sexual reproduction to apomictic parthenogenesis in Timema stick insects. Evolution, 63(1), 84-103. 
https://doi.org/10.1111/j.1558-5646.2008.00524.x

Simon, J.-C., Delmotte, F., Rispe, C., & Crease, T. (2003). Phylogenetic relationships between parthenogens and their sexual relatives: the possible routes to parthenogenesis in animals. Biological Journal of the Linnean Society, 79(1), 151-163. https://doi.org/10.1046/j.1095-8312.2003.00175.x

Larose, C., Lavanchy,  G., Freitas, S., Parker, D.J., Schwander, T. (2023) Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects? bioRxiv, 2022.03.25.485836, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.03.25.485836

Facultative parthenogenesis: a transient state in transitions between sex and obligate asexuality in stick insects?Chloé Larose, Guillaume Lavanchy, Susana Freitas, Darren J. Parker, Tanja Schwander<p>Transitions from obligate sex to obligate parthenogenesis have occurred repeatedly across the tree of life. Whether these transitions occur abruptly or via a transient phase of facultative parthenogenesis is rarely known. We discovered and char...Reproduction and SexTrine Bilde2022-05-20 10:41:13 View
25 Jan 2024
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Sperm production and allocation in response to risk of sperm competition in the black soldier fly Hermetia illucens

Elevated sperm production and faster transfer: plastic responses to the risk of sperm competition in males of the black sodier fly Hermetia illuce

Recommended by ORCID_LOGO based on reviews by Rebecca Boulton, Isabel Smallegange and 1 anonymous reviewer

In this paper (Manas et al., 2023), the authors investigate male responses to risk of sperm competition in the black soldier fly Hermetia illuce, a widespread insect that has gained recent attention for its potential to be farmed for sustainable food production (Tomberlin & van Huis, 2020).

Using an experimental approach that simulated low-risk (males were kept individually) and high-risk (males were kept in groups of 10) of sperm competition, they found that males reared in groups showed a significant increase in sperm production compared with males reared individually. This shows a response to the rearing environment in sperm production that is consistent with an increase in the perceived risk of sperm competition.

These males were then used in mating experiments to determine whether sperm allocation to females during mating was influenced by the perceived risk of sperm competition. Mating experiments were initiated in groups, since mating only occurs when more than one male and one female are present, indicating strong sexual selection in the wild. Once a copulation began, the pair was moved to a new environment with no competition, with male competitors, or with other females, to test how social environment and potentially the sex of surrounding individuals influenced sperm allocation during mating. Copulation duration and the number of sperm transferred were subsequently counted.

In these mating experiments, the number of sperm stored in the female spermathecae increased under immediate risk of sperm competition. Interestingly, this was not because males copulated for longer depending on the risk of sperm competition, indicating that males respond plastically to the risk of competition by elevating their investment in sperm production and speed of sperm transfer. There was no difference between competitive environments consisting of males or females respectively, suggesting that it is the presence of other flies per se that influence sperm allocation.

The study provides an interesting new example of how males alter reproductive investment in response to social context and sexual competition in their environment. In addition, it provides new insights into the reproductive biology of the black soldier fly Hermetia illucens, which may be relevant for optimizing farming conditions.

References

Manas F, Labrousse C, Bressac C (2023) Sperm production and allocation in response to risks of sperm competition in the black soldier fly Hermetia illucens. bioRxiv, 2023.06.20.544772, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology.  https://doi.org/10.1101/2023.06.20.544772

Tomberlin JK, Van Huis A (2020) Black soldier fly from pest to ‘crown jewel’ of the insects as feed industry: an historical perspective. Journal of Insects as Food and Feed, 6, 1–4. https://doi.org/10.3920/JIFF2020.0003

Sperm production and allocation in response to risk of sperm competition in the black soldier fly Hermetia illucensFrédéric Manas, Carole Labrousse, Christophe Bressac<p style="text-align: justify;">In polyandrous species, competition between males for offspring paternity goes on after copulation through the competition of their ejaculates for the fertilisation of female's oocytes. Given that males allocating m...Reproduction and Sex, Sexual SelectionTrine Bilde2023-06-26 09:41:07 View
16 Mar 2017
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Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection

Measurement of sexual selection in plants made easier

Recommended by and

Sexual selection occurs in flowering plants too. However it tends to be understudied in comparison to animal sexual selection, in part because the minuscule size and long dispersal distances of the individuals producing male gametes (pollen grains) seriously complicate the estimation of male siring success and thereby the measurement of sexual selection. Dorken and Perry [1] introduce a novel and clever approach to estimate sexual selection in plants, which bypasses the need for a direct quantification of absolute male mating success. This approach builds on the fact that the strength of sexual selection is directly related to the ability of individuals to monopolize mates [2]. In plants, mate monopolization can be assessed by examining the proportion of seeds produced by a given plant that are full-sibs, i.e. that share the same father. A nice feature of this proportion of full-sib seeds per maternal parent is it equals the coefficient of correlated paternity of Ritland [3], which can be readily obtained from the hundreds of plant mating system studies using genetic markers. A less desirable feature of the proportion of full sibs per maternal plant is that it is inversely related to population size, an effect that should be corrected for. The resulting index of mate monopolization is a simple product: (coefficient of correlated paternity)x(population size – 1). The authors test whether their index of mate monopolization is a good correlate of sexual selection, measured more traditionally as the selection differential on a trait influencing mating success, using a combination of theoretical and experimental approaches. Both approaches confirm that the two quantities are positively correlated, which suggests that the index of mate monopolization could be a convenient way to estimate the relative strength of sexual selection in flowering plants. These results call for further investigation, e.g. to verify that the effect of population size is well controlled for, or to assess the effects of non-random mating and inbreeding depression; however, this work paves the way for an expansion of sexual selection studies in flowering plants.

References

[1] Dorken ME and Perry LE. 2017. Correlated paternity measures mate monopolization and scales with the magnitude of sexual selection. Journal of Evolutionary Biology 30: 377-387 doi: 10.1111/jeb.13013

[2] Klug H, Heuschele J, Jennions M and Kokko H. 2010. The mismeasurement of sexual selection. Journal of Evolutionary Biology 23:447-462. doi: 10.1111/j.1420-9101.2009.01921.x

[3] Ritland K. 1989. Correlated matings in the partial selfer Mimulus guttatus. Evolution 43:848-859. doi: 10.2307/2409312

Correlated paternity measures mate monopolization and scales with the magnitude of sexual selectionDorken, ME and Perry LEIndirect measures of sexual selection have been criticized because they can overestimate the magnitude of selection. In particular, they do not account for the degree to which mating opportunities can be monopolized by individuals of the sex that ...Sexual SelectionEmmanuelle Porcher2017-03-13 23:22:26 View