A comprehensive study by Roux et al 2024 investigates the impact of eusociality on the efficacy of natural selection in termites, with and additional focus on whether higher levels of social complexity are associated with lower effective population size (Ne) and relaxed purifying selection.

Eusociality is characterized by a division of reproductive labor, cooperative care of offspring, and overlapping generations, and has evolved independently across various animal taxa with the most complex social systems found in Hymenoptera (bees, wasps, ants) and termites. Because reproduction is limited to a few individuals, this leads to a reduced effective population size (Ne), which impacts genome evolution. Smaller Ne increases the influence of genetic drift, weakening the efficiency of natural selection and allowing the accumulation of weakly deleterious mutations. This phenomenon, known as the "drift barrier," alters the mutation-selection balance in eusocial organisms.

Studies in a range of social arthropods including ants, termites, crustaceans and spiders have shown an elevated ratio of nonsynonymous to synonymous substitutions (dN/dS), indicating relaxed purifying selection due to small Ne. In termite species with complex social structures, such as those with large colonies and high caste specialization, there are reports of higher dN/dS ratios compared to simpler social species. This suggests that higher social complexity, reflected in traits like nesting strategies and developmental pathways, further reduces Ne and the effectiveness of natural selection. 

The authors address these hypotheses by exploring the genomic impact of eusociality in termites (Isoptera) taking two approaches: First, they analyze transcriptome data from 66 Blattodea species and calculate the ratio of non-synonymous to synonymous mutations (dN/dS) as an indicator of natural selection efficiency and effective population size. They analyses reveal an increased dN/dS ratio in termites compared to other Blattodea species, reinforcing the notion that convergent evolution toward eusociality significantly reduces effective population size and weakens natural selection efficiency across the genome. Additionally, a comparison of 68 termite transcriptomes shows that this effect is more pronounced in species with higher social complexity. This is exciting as it advances our understanding of how increasing complexity in social organization decreases Ne and the efficiency of natural selection. The study substantiates the notion that social transitions follow evolutionary trajectories where lower and Ne and increasing drift have negative consequences for genome evolution (Ma et al 2024).

References

Camille Roux, Alice Ha, Arthur Weyna, Morgan Lode, Jonathan Romiguier (2024) The impact of social complexity on the efficacy of natural selection in termites. bioRxiv, ver.2 peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.1101/2024.04.26.591327

Jilong Ma, Jesper Bechsgaard, Anne Aagaard, Palle Villesen, Trine Bilde, Mikkel Heide Schierup (2024) Sociality in spiders is an evolutionary dead-end. 
bioRxiv 2024.04.22.590577. https://doi.org/10.1101/2024.04.22.590577

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

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

In mammals, it is well documented that sexual dimorphism and in particular sex differences in behaviour are fine-tuned by gonadal hormonal profiles. For example, in lemurs, where female social dominance is common, the level of testosterone in females is unusually high compared to that of other primate females (Petty and Drea 2015). 

Recent studies however suggest that gonadal hormones might not be the only biological factor involved in establishing sexual dimorphism, sex chromosomes might also play a role. The four core genotype (FCG) model and other similar systems allowing to decouple phenotypic and genotypic sex in mice have provided very convincing evidence of such a role (Gatewood et al. 2006; Arnold and Chen 2009; Arnold 2020a, 2020b). This however is a new field of research and the role of sex chromosomes in establishing sexually dimorphic behaviours has not been studied very much yet. Moreover, the FCG model has some limits. Sry, the male determinant gene on the mammalian Y chromosome might be involved in some sex differences in neuroanatomy, but Sry is always associated with maleness in the FCG model, and this potential role of Sry cannot be studied using this system.

Heitzmann et al. have used a natural system to approach these questions. They worked on the African Pygmy mouse, Mus minutoides, in which a modified X chromosome called X* can feminize X*Y individuals, which offers a great opportunity for elegant experiments on the effects of sex chromosomes versus hormones on behaviour. They focused on maternal care and compared pup retrieval, nest quality, and mother-pup interactions in XX, X*X and X*Y females. They found that X*Y females are significantly better at retrieving pups than other females. They are also much more aggressive towards the fathers than other females, preventing paternal care. They build nests of poorer quality but have similar interactions with pups compared to other females. Importantly, no significant differences were found between XX and X*X females for these traits, which points to an effect of the Y chromosome in explaining the differences between X*Y and other females (XX, X*X). Also, another work from the same group showed similar gonadal hormone levels in all the females (Veyrunes et al. 2022). 

Heitzmann et al. made a number of predictions based on what is known about the neuroanatomy of rodents which might explain such behaviours. Using cytology, they looked for differences in neuron numbers in the hypothalamus involved in the oxytocin, vasopressin and dopaminergic pathways in XX, X*X and X*Y females, but could not find any significant effects. However, this part of their work relied on very small sample sizes and they used virgin females instead of mothers for ethical reasons, which greatly limited the analysis. 

Interestingly, X*Y females have a higher reproductive performance than XX and X*X ones, which compensate for the cost of producing unviable YY embryos and certainly contribute to maintaining a high frequency of X* in many African pygmy mice populations (Saunders et al. 2014, 2022). X*Y females are probably solitary mothers contrary to other females, and Heitzmann et al. have uncovered a divergent female strategy in this species. Their work points out the role of sex chromosomes in establishing sex differences in behaviours. 

References

Arnold AP (2020a) Sexual differentiation of brain and other tissues: Five questions for the next 50 years. Hormones and Behavior, 120, 104691. https://doi.org/10.1016/j.yhbeh.2020.104691

Arnold AP (2020b) Four Core Genotypes and XY* mouse models: Update on impact on SABV research. Neuroscience & Biobehavioral Reviews, 119, 1–8. https://doi.org/10.1016/j.neubiorev.2020.09.021

Arnold AP, Chen X (2009) What does the “four core genotypes” mouse model tell us about sex differences in the brain and other tissues? Frontiers in Neuroendocrinology, 30, 1–9. https://doi.org/10.1016/j.yfrne.2008.11.001

Gatewood JD, Wills A, Shetty S, Xu J, Arnold AP, Burgoyne PS, Rissman EF (2006) Sex Chromosome Complement and Gonadal Sex Influence Aggressive and Parental Behaviors in Mice. Journal of Neuroscience, 26, 2335–2342. https://doi.org/10.1523/JNEUROSCI.3743-05.2006

Heitzmann LD, Challe M, Perez J, Castell L, Galibert E, Martin A, Valjent E, Veyrunes F (2022) Genotypic sex shapes maternal care in the African Pygmy mouse, Mus minutoides. bioRxiv, 2022.04.05.487174, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.04.05.487174

Petty JMA, Drea CM (2015) Female rule in lemurs is ancestral and hormonally mediated. Scientific Reports, 5, 9631. https://doi.org/10.1038/srep09631

Saunders PA, Perez J, Rahmoun M, Ronce O, Crochet P-A, Veyrunes F (2014) Xy Females Do Better Than the Xx in the African Pygmy Mouse, Mus Minutoides. Evolution, 68, 2119–2127. https://doi.org/10.1111/evo.12387

Saunders PA, Perez J, Ronce O, Veyrunes F (2022) Multiple sex chromosome drivers in a mammal with three sex chromosomes. Current Biology, 32, 2001-2010.e3. https://doi.org/10.1016/j.cub.2022.03.029

Veyrunes F, Perez J, Heitzmann L, Saunders PA, Givalois L (2022) Separating the effects of sex hormones and sex chromosomes on behavior in the African pygmy mouse Mus minutoides, a species with XY female sex reversal. bioRxiv, 2022.07.11.499546. https://doi.org/10.1101/2022.07.11.499546

Genetic diversity is a key aspect of biodiversity and has important implications for evolutionary potential and thereby the persistence of species. Improving our understanding of the factors that drive genetic structure within and between populations is, therefore, a long-standing goal in evolutionary biology. However, this is a major challenge, because of the complex interplay between genetic drift, migration, and extinction/colonization dynamics on the one hand, and the biology and ecology of species on the other hand (Romiguier et al. 2014, Ellegren and Galtier 2016, Charlesworth 2003). 

Jarne et al. (2021) studied whether environmental and demographic factors affect the population genetic structure of four species of hermaphroditic freshwater snails in a similar way, using comparative analyses of neutral genetic microsatellite markers. 

Specifically, they investigated microsatellite variability of Hygrophila in almost 280 sites in Guadeloupe, Lesser Antilles, as part of a long-term survey experiment (Lamy et al. 2013). They then modelled the influence of the mating system, local environmental characteristics and demographic factors on population genetic diversity.

Consistent with theoretical predictions (Charlesworth 2003), they detected higher genetic variation in two outcrossing species than in two selfing species, emphasizing the importance of the mating system in maintaining genetic diversity. The study further identified an important role of site connectivity, through its influences on effective population size and extinction/colonisation events. Finally, the study detects an influence of interspecific interactions caused by an ongoing invasion by one of the studied species on genetic structure, highlighting the indirect effect of changes in community composition and demography on population genetics.

Jarne et al. (2021) could address the extent to which genetic structure is determined by demographic and environmental factors in multiple species given the remarkable sampling available. Additionally, the study system is extremely suitable to address this hypothesis as species’ habitats are defined and delineated. Whilst the authors did attempt to test for across-species correlations, further investigations on this matter are required. Moreover, the effect of interactions between factors should be appropriately considered in any modelling between genetic structure and local environmental or demographic features.

The findings in this study contribute to improving our understanding of factors influencing population genetic diversity, and highlights the complexity of interacting factors, therefore also emphasizing the challenges of drawing general implications, additionally hampered by the relatively limited number of species studied. Jarne et al. (2021) provide an excellent showcase of an empirical framework to test determinants of genetic structure in natural populations. As such, this study can be an example for further attempts of comparative analysis of genetic diversity.

References

Charlesworth, D. (2003) Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358, 1051-1070. doi: https://doi.org/10.1098/rstb.2003.1296

Ellegren, H. and Galtier, N. (2016) Determinants of genetic diversity. Nature Reviews Genetics, 17, 422-433. doi: https://doi.org/10.1038/nrg.2016.58

Jarne, P., Lozano del Campo, A., Lamy, T., Chapuis, E., Dubart, M., Segard, A., Canard, E., Pointier, J.-P. and David, P. (2021) Connectivity and selfing drives population genetic structure in a patchy landscape: a comparative approach of four co-occurring freshwater snail species. HAL, hal-03295242, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://hal.archives-ouvertes.fr/hal-03295242

Lamy, T., Gimenez, O., Pointier, J. P., Jarne, P. and David, P. (2013). Metapopulation dynamics of species with cryptic life stages. The American Naturalist, 181, 479-491. doi: https://doi.org/10.1086/669676

Romiguier, J., Gayral, P., Ballenghien, M. et al. (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261-263. doi: https://doi.org/10.1038/nature13685

The role of microbial symbionts in governing social traits of their hosts is an exciting and developing research area. Just like symbionts influence host reproductive behaviour and can cause mating incompatibilities to promote symbiont transmission through host populations (Engelstadter and Hurst 2009; Correa and Ballard 2016; Johnson and Foster 2018) (see also discussion on conflict resolution in Johnsen and Foster 2018), microbial symbionts could enhance transmission by promoting the social behaviour of their hosts (Ezenwa et al. 2012; Lewin-Epstein et al. 2017; Gurevich et al. 2020). Here I apply the term ‘symbiosis’ in the broad sense, following De Bary 1879 as “the living together of two differently named organisms“ independent of effects on the organisms involved (De Bary 1879), i.e. the biological interaction between the host and its symbionts may include mutualism, parasitism and commensalism.
So far, we have relative few studies that explore the role of symbionts in promoting social behaviours such as parental care. Clearly, disentangling cause and effect when assessing the functional significance of symbiotic relationships in general is extremely challenging, and perhaps even more caution is needed when assessing the role of symbionts in the evolution of parental care, given the high fitness benefits to the offspring of receiving care. An interesting study on the symbiotic relationship between termites and their eukaryotic gut symbionts proposes a role of gut flagellates in the origin of subsocial behaviour (extended offspring care) in the termites through proctodeal trophallaxis (i.e. anus-to-mouth feeding), driven by mutualistic beneficial interactions (Nalepa 2020). Van Meyel et al. (2021) hypothesized a role of gut symbionts in promoting maternal care behaviour in the European earwig, and set out to test this idea in a carefully executed experimental study. They used a broad-spectrum antibiotic treatment to alter gut microbiota in mothers and examined its effect on maternal care provisioning. While the antibiotic treatment altered the gut microbiome, no effect on pre- or post-hatching maternal care was detected. The authors also investigated a broad range of physiological and reproductive traits measured over a major part of a female’s lifetime, and detected no effect of microbiome alteration on these traits. The study therefore does not provide evidence for a direct role of the gut microbiome in shaping offspring care in this population of European earwigs.
Within populations, earwigs show inter-individual variation in the expression of maternal care (Meunier et al. 2012; Ratz et al. 2016), and there is evidence that genetic and environmental factors contribute to this this variation (Meunier and Kolliker 2012; Kramer et al. 2017). The study by Van Meyel et al. (2021) is the first to analyse microbiome composition of the European earwig, and they study host-symbiont associations in a single population. A next step could be to explore among population variation in the gut microbiome, to achieve a better understanding on host-microbiome variation and dynamics in wild populations. Depending on the nature of host-symbiont associations across populations, new perspectives on their functional significance may arise (Hird 2017; Johnson and Foster 2018). It is therefore too early to conclusively confirm or reject the role of microbial symbionts in the expression of parental care in this system.

References

Correa, C. C., and Ballard, J. W. O. (2016). Wolbachia associations with insects: winning or losing against a master manipulator. Frontiers in Ecology and Evolution, 3, 153. doi: https://doi.org/10.3389/fevo.2015.00153

De Bary, A. (1879). Die Erscheinung der Symbiose. Verlag von Karl J. Trubner, Strassburg.

Engelstädter, J., and Hurst, G. D. (2009). The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics, 40, 127-149. doi: https://doi.org/10.1146/annurev.ecolsys.110308.120206

Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M., and Xavier, J. B. (2012). Animal behavior and the microbiome. Science, 338(6104), 198-199. doi: https://doi.org/10.1126/science.1227412

Gurevich, Y., Lewin-Epstein, O., and Hadany, L. (2020). The evolution of paternal care: a role for microbes?. Philosophical Transactions of the Royal Society B, 375(1808), 20190599. doi: https://doi.org/10.1098/rstb.2019.0599

Hird, S. M. (2017). Evolutionary biology needs wild microbiomes. Frontiers in microbiology, 8, 725. doi: https://doi.org/10.3389/fmicb.2017.00725

Johnson, K. V. A., and Foster, K. R. (2018). Why does the microbiome affect behaviour?. Nature reviews microbiology, 16(10), 647-655. doi: https://doi.org/10.1038/s41579-018-0014-3

Kramer et al. (2017). When earwig mothers do not care to share: parent–offspring competition and the evolution of family life. Functional Ecology, 31(11), 2098-2107. doi: https://doi.org/10.1111/1365-2435.12915

Lewin-Epstein, O., Aharonov, R., and Hadany, L. (2017). Microbes can help explain the evolution of host altruism. Nature communications, 8(1), 1-7. doi: https://doi.org/10.1038/ncomms14040

Meunier, J., and Kölliker, M. (2012). Parental antagonism and parent–offspring co-adaptation interact to shape family life. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 3981-3988. doi: https://doi.org/10.1098/rspb.2012.1416

Meunier, J., Wong, J. W., Gómez, Y., Kuttler, S., Röllin, L., Stucki, D., and Kölliker, M. (2012). One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evolutionary Ecology, 26(3), 669-682. doi: https://doi.org/10.1007/s10682-011-9510-x

Nalepa, C. A. (2020). Origin of mutualism between termites and flagellated gut protists: transition from horizontal to vertical transmission. Frontiers in Ecology and Evolution, 8, 14. doi: https://doi.org/10.3389/fevo.2020.00014

Ratz, T., Kramer, J., Veuille, M., and Meunier, J. (2016). The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care. Oecologia, 182(2), 443-452. doi: https://doi.org/10.1007/s00442-016-3685-3

Van Meyel, S., Devers, S., Dupont, S., Dedeine, F. and Meunier, J. (2021) Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig. bioRxiv, 2020.10.08.331363. ver. 5 peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.1101/2020.10.08.331363