Despite advances in genomic research, many views of genome evolution are still based on what we know from a handful of species, such as humans. This also applies to our knowledge of sex chromosomes. We've apparently been too much used to the situation in which a highly degenerate Y chromosome coexists with an almost normal X chromosome to be able to fully grasp all the questions implied by this situation. Lately, many more sex chromosomes have been studied in other organisms, such as in plants, and the view is changing radically: there is a large diversity of situations, ranging from young highly divergent sex chromosomes to old ones that are so similar that they're hard to detect. Undoubtedly inspired by these recent findings, a few theoretical studies have been published around 2 years ago that put an entirely new light on the evolution of sex chromosomes. The differences between these models have however remained somewhat difficult to appreciate by non-specialists. 

In particular, the models by Lenormand & Roze (2022) and by Jay et al. (2022) seemed quite similar. Indeed, both rely on the same mechanism for initial recombination suppression: a ``lucky'' inversion, i.e. one with less deleterious mutations than the population average, encompassing the sex-determination locus, is initially selected. However, as it doesn't recombine, it will quickly accumulate deleterious mutations lowering its fitness. And it's at this point the models diverge: according to Lenormand & Roze (2022), nascent dosage compensation not only limits the deleterious effects on fitness by the ongoing degeneration, but it actually opposes recombination restoration as this would lead gene expression away from the optimum that has been reached. On the other hand, in the model by Jay et al. (2022), no additional ingredient is required: they argue that once an inversion had been fixed, reversions that restore recombination are extremely unlikely.

This is what Lenormand & Roze (2024) now call a ``constraint'': in Jay et al.'s model, recombination restoration is impossible for mechanistic reasons. Lenormand & Roze (2024) argue such constraints cannot explain long-term recombination suppression. Instead, a mechanism should evolve to limit the negative fitness effects of recombination arrest, otherwise recombination is either restored, or the population goes extinct due to a dramatic drop in the fitness of the heterogametic sex. These two arguments work together: given the huge fitness cost of the lack of ongoing degeneration of the non-recombining Y, in the absence of compensatory mechanisms, there is a very strong selection for the restoration of recombination, so that even when restoration a priori is orders of magnitude less likely than inversion (leading to recombination suppression), it will eventually happen. 

One way the negative fitness effects of recombination suppression can be limited, is the way the authors propose in their own model: dosage compensation evolves through regulatory evolution right at the start of recombination suppression. This changes our classical, simplistic view that dosage compensation evolves in response to degeneration: rather, Lenormand & Roze (2024) argue, that degeneration can only happen when dosage compensation is effective.

The reasoning is convincing and exposes the difference between the models to readers without a firm background in mathematical modelling. Although Lenormand & Roze (2024) target the "constraint theory", it seems likely that other theories for the maintenance of recombination suppression that don't imply the compensation of early degeneration are subject to the same criticism. Indeed, they mention the widely-cited "sexual antagonism" theory, in which mutations with a positive effect in males but a negative in females will select for recombination suppression that will link them to the sex-determining gene on the Y. However, once degeneration starts, the sexually-antagonistic benefits should be huge to overcome the negative effects of degeneration, and it's unlikely they'll be large enough.

A convincing argument by Lenormand & Roze (2024) is that there are many ways recombination could be restored, allowing to circumvent the possible constraints that might be associated with reverting an inversion. First, reversions don't have to be exact to restore recombination. Second, the sex-determining locus can be transposed to another chromosome pair, or an entirely new sex-determining locus might evolve, leading to sex-chromosome turnover which has effectively been observed in several groups.

These modelling studies raise important questions that need to be addressed with both theoretical and empirical work. First, is the regulatory hypothesis proposed by Lenormand & Roze (2022) the only plausible mechanism for the maintenance of long-term recombination suppression? The female- and male-specific trans regulators of gene expression that are required for this model, are they readily available or do they need to evolve first? Both theoretical work and empirical studies of nascent sex chromosomes will help to answer these questions. However, nascent sex chromosomes are difficult to detect and dosage compensation is difficult to reveal.

Second, how many species today actually have "stable" recombination suppression? Maybe many species are in a transient phase, with different populations having different inversions that are either on their way to being fixed or starting to get counterselected. The models have now shown us some possibilities qualitatively but can they actually be quantified to be able to fit the data and to predict whether an observed case of recombination suppression is transient or stable? 

The debate will continue, and we need the active contribution of theoretical biologists to help clarify the underlying hypotheses of the proposed mechanisms. 

Conflict of interest statement: I did co-author a manuscript with D. Roze in 2023, but do not consider this a conflict of interest. The manuscript is the product of discussions that have taken place in a large consortium mainly in 2019. It furthermore deals with an entirely different topic of evolutionary biology.

References

Jay P, Tezenas E, Véber A, and Giraud T. (2022) Sheltering of deleterious mutations explains the stepwise extension of recombination suppression on sex chromosomes and other supergenes. PLoS Biol.;20:e3001698. https://doi.org/10.1371/journal.pbio.3001698
 
Lenormand T and Roze D. (2022) Y recombination arrest and degeneration in the absence of sexual dimorphism. Science;375:663-6. https://doi.org/10.1126/science.abj1813
 
Lenormand T and Roze D. (2024) Can mechanistic constraints on recombination reestablishment explain the long-term maintenance of degenerate sex chromosomes? bioRxiv, ver. 5 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.02.17.528909

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

Many species with separate sexes have evolved sex chromosomes, with the sex-limited chromosomes (i.e. the Y or W chromosomes) exhibiting a wide range of genetic divergences from their homologous X or Z chromosomes (Bachtrog et al., 2014). Variable divergences can result from the cessation of recombination between sex chromosomes that occurred at different time points, with the mechanisms of initiation and expansion of recombination suppression along sex chromosomes remaining poorly understood (Charlesworth, 2017). 

The study by Castel et al (2023) describes the serendipitous discovery of a shared XY sex chromosome system in three closely related hydrothermal vent gastropods. The X and Y chromosomes appear to still recombine but at variable rates across the three species. This variation makes the gastropod system a very promising focus for future research on sex chromosome evolution. 

An additional intriguing finding is that some females in one of three gastropod species contain male reproductive tissue in their gonads, providing a fascinating case of a mixed or transitory sexual system. Overall, the study by Castel et al (2023) offers the first insights into the reproduction and sex chromosome system of animals living in deep marine vents, which have remained poorly studied and open outstanding research perspectives on these creatures.

References

Bachtrog, D., J.E.Mank, C.L.Peichel, M.Kirkpatrick, S.P.Otto, T.L. Ashman, M.W.Hahn, J.Kitano, I.Mayrose, R.Ming, et al. 2014.Sex determination: why so many ways of doing it? PLoSBiol. 12:e1001899. https://doi.org/10.1371/journal.pbio.1001899

Charlesworth, D. Young sex chromosomes in plants and animals. 2019. New Phytologist 224: 1095–1107. https://doi.org/10.1111/nph.16002

Castel J, Pradillon F, Cueff V, Leger G, Daguin-Thiébaut C, Ruault S, Mary J, Hourdez S, Jollivet D, and Broquet T 2023. Genetic sex determination in three closely related hydrothermal vent gastropods, including one species with intersex individuals. bioRxiv, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.04.11.536409

What does it mean to be highly social?  Considering the so-called four ‘pinnacles’ of animal society (Wilson, 1975) – humans, cooperative breeding as found in some non-human mammals and birds, the social insects, and colonial marine invertebrates – having inter-individual relations extending beyond the sexual pair and the parent-offspring interaction is foremost.  In many cases being social implies a high local population density, interaction with the same group of individuals over an extended time period, and an overlapping of generations.  Additional features of social species may be a wide geographical range, perhaps associated with ecological and behavioral plasticity, the latter often facilitated by cultural transmission of traditions.  

Narrowing our perspective to the domain of PCI Evolutionary Biology, we might continue our question by asking whether being social predisposes one to a special evolutionary path toward the future.  Do social species evolve faster (or slower) than their more solitary relatives such that over time they are more unlike (or similar to) those relatives (anagenesis)?  And are evolutionary changes in social species more or less likely to be accompanied by lineage splitting (cladogenesis) and ultimately speciation?  The latter question is parallel to one first posed over 40 years ago (West-Eberhard, 1979; Lande, 1981) for sexually selected traits:  Do strong mating preferences and conspicuous courtship signals generate speciation via the Fisherian process or ecological divergence?  An extensive survey of birds had found little supporting evidence (Price, 1998), but a recent one that focused on plumage complexity in tanagers did reveal a relationship, albeit a weak one (Price-Waldman et al., 2020).  Because sexual selection has been viewed as a part of the broader process of social selection (West-Eberhard, 1979), it is thus fitting to extend our surveys to the evolutionary implications of being social.

Unlike the inquiry for a sexual selection - evolutionary change connection, a social behavior counterpart has remained relatively untreated.  Diverse logistical problems might account for this oversight.  What objective proxies can be used for social behavior, and for the rate of evolutionary change within a lineage?  How many empirical studies have generated data from which appropriate proxies could be extracted?  More intractable is the conundrum arising from the connectedness between socially- and sexually-selected traits.  For example, the elevated population density found in highly social species can greatly increase the mating advantage enjoyed by an attractive male.  If anagenesis is detected, did it result from social behavior or sexual selection?  And if social behavior leads to a group structure in which male-male competition is reduced, would a modest rate of evolutionary change be support for the sexual selection - evolutionary speed connection or evidence opposing the sociality - evolution one?

Against the above odds, several biologists have begun to explore the notion that social behavior just might favor evolutionary speed in either anagenesis or cladogenesis.  In a recent analysis relying on the comparative method, Lluís Socias-Martínez and Louise Rachel Peckre (2023) combed the scientific literature archives and identified those studies with specific data on the relationships between sexual selection or social behavior and evolutionary change, either anagenesis or cladogenesis.  The authors were careful to employ fairly conservative criteria for including studies, and the number eventually retained was small.  Nonetheless, some patterns emerge:  Many more studies report anagenesis than cladogenesis, and many more report correlations with sexually-selected traits than with non-sexual social behavior ones.  And, no study indicates a potential effect of social behavior on cladogenesis.  Is this latter observation authentic or an artifact of a paucity of data?  There are some a priori reasons why cladogenesis may seldom arise.  Whereas highly social behavior could lead to fission encompassing mutually isolated population clusters within a species, social behavior may also engender counterbalancing plasticity that allows and even promotes inter-cluster migration and fusion.  And briefly – and non-systematically, as the rate of lineage splitting would need to be measured – looking at one of the pinnacles of animal social behavior, the social insects, there is little indication that diversification has been accelerated.  There are fewer than 3000 described species of termites, only ca. 16,000 ants, and the vast majority of bees and wasps are solitary.                            

Lluís Socias-Martínez and Louise Rachel Peckre provide us with a very detailed discussion of these and a myriad of other complications.  I end with a common refrain, we need more consideration of the authors’ interesting question, and much more data and analysis.  One can thank Socias-Martínez and Peckre for pointing us in that direction.

References

Lande, R. (1981). Models of speciation by sexual selection on polygenic traits. Proc. Natn. Acad. Sci. USA 78, 3721-3725. https://doi.org/10.1073/pnas.78.6.3721

Price, T. (1998). Sexual selection and natural selection in bird speciation. Phil. Trans. Roy. Soc. B, 353, 251-260.  https://doi.org/10.1098/rstb.1998.0207  

Price‐Waldman, R. M., Shultz, A. J., & Burns, K. J. (2020). Speciation rates are correlated with changes in plumage color complexity in the largest family of songbirds. Evolution, 74(6), 1155–1169. https://doi.org/10.1111/evo.13982

Socias-Martínez and Peckre. (2023). Does sociality affect evolutionary speed? Zenodo, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.5281/zenodo.10086186

West-Eberhard, M. J. (1979). Sexual selection, social competition, and evolution. Proceedings of the American Philosophical Society, 123(4), 222–234. http://www.jstor.org/stable/2828804

Wilson, E. O. (1975). Sociobiology. The New Synthesis. Cambridge, Mass., The Belknap Press of Harvard University

The striking differences in species richness among lineages in the Tree of Life have long attracted much research interest. In particular, researchers have asked whether certain traits are associated with greater diversification, with a particular focus on traits under sexual selection given their direct link to mating isolation.

Polymorphism, defined as the presence of co-occurring, heritable morphs within a population, has been proposed to influence diversification rates although the effect has been proposed as both promoting or alternatively impeding speciation. The effect of polymorphism may be positive, that is facilitating speciation if polymorphism allows to broaden the ecological niche, thus enabling range expansion, or enabling maintenance of populations in variable environments. Specialized ectomorphs have been observed in several species (e.g. Kusche et al. 2015, Lattanzio and Miles 2016, Whitney et al. 2018, Scali et al. 2016). Polymorphism may also facilitate speciation if a morph is lost during the colonization of a novel area or niche, resulting in rapid divergence of the remaining morphs and reproductive isolation from the ancestral population, known as the morph speciation hypothesis (West-Eberhard 1986, Corl et al. 2010). On the other hand, polymorphism may hamper speciation through disassortative maintaining by morph, which may maintain the polymorphism through the speciation process (Jamie and Meier 2020). An example of such a process is Heliconius numata where disassortative mate preferences based on color hampers ecological speciation (Chouteau et al. 2017). Previous evidence in birds and lizards suggests polymorphism favors diversification (Corl et al. 2010b, 2012, Hugall and Stuart-Fox 2012, Brock et al. 2021).

Here, de Solan et al. (2023) test the effect of polymorphism on diversification in Lacertidae, a family of lizards containing more than 300 species distributed across Europe, Africa and Asia. The group offers a good model system to test the effect of polymorphism on speciation as it contains several species with colour polymorphism, sometimes present in both sexes but restricted to males when present in the flank. Using coloration data from the literature as well as photographs of live specimens for 295 species the authors tested whether the presence of polymorphism is associated with higher diversification rates.

While undertaking their project, another group independently tackled the same question (Brock et al. 2021), using the same model system but coming to very different conclusions. Therefore, de Solan et al. (2023) decided to also contrast their results with those of Brock et al. (2021) to determine the factors responsible for the contrasting results of both studies. The latter I consider one of the strengths of the work, given the careful re-analyses to determine the causes of the discrepancies between both studies. De Solan et al. (2023) found no association between the presence of polymorphism and diversification rates, even though they used different analytical approaches. Thus, this study is interesting as it provides results that do not support a positive effect of polymorphism on species richness. The use of a phylogeny with more limited species sampling (García-Porta et al. 2019) implied that the authors had to manually add 75 species, of which 17 were added to the tree based on information from previously published trees and 68 were added at random locations within the genus. To control for potential biases the authors repeated the analyses using a sample of trees with the imputed taxa, results were broadly concordant across the set of trees. The careful re-analysis contrasting Brock et al. (2021) and de Solan et al. (2023) results suggests the difference is mainly due to a difference in how species were coded as presenting polymorphism, which differed between the two studies, as well as a difference in the package version used to run the state-dependent diversification models. Interestingly non-parametric analyses yielded similar results across both datasets. 
 
References
 
Brock, K.M., McTavish, E.J., Edwards, D.L. 2021. Colour polymorphism is a driver of diversification in the lizard family Lacertidae. Systematic Biology. 71: 24-39. https://doi.org/10.1093/sysbio/syab046
 
Chouteau, M., Llaurens, V., Piron-Prunier, F., Joron, M. 2017. Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures. Proceedings of the National Academy of Sciences. 114: 8325-8329. https://doi.org/10.1073/pnas.1702482114
 
Corl, A., Davis, A.R., Kuchta, S.R., Comendant, T., Sinervo, B. 2010a. Alternative mating strategies and the evolution of sexual dimorphism in the side-blotched lizard, Uta stansburiana: a population-level comparative analysis. Evolution. 64: 79-96. https://doi.org/10.1111/j.1558-5646.2009.00791.x 
 
Corl, A., Davis, A.R., Kuchta, S.R., Sinervo, B. 2010b. Selective loss of polymorphic mating types is associated with rapid phenotypic evolution during morphic speciation. Proceedings of the National Academy of Sciences. 107: 4254-4259. https://doi.org/10.1073/pnas.0909480107
 
Corl, A., Lancaster, L.T., Sinervo, B. 2012. Rapid formation of reproductive isolation between two populations of side-blotched lizards, Uta stansburiana. Copeia. 2012: 593-602. https://doi.org/10.1643/CH-11-166

Garcia-Porta, J., Irisarri, I., Kirchner, M. et al. 2019. Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards. Nature Communications. 10: 4077. https://doi.org/10.1038/s41467-019-11943-x
 
Hugall, A.F., Stuart-Fox, D. 2012. Accelerated speciation in colour-polymorphic birds. Nature. 485: 631-634. https://doi.org/10.1038/nature11050
 
Jamie, G.A. and Meier, J.I. 2020. The persistence of polymorphisms across species radiations. Trends in Ecology and Evolution. 35: 795-808. https://doi.org/10.1016/j.tree.2020.04.007
 
Kusche, H., Elmer, K.R., Meyer, A. 2015. Sympatric ecological divergence associated with a colour polymorphism. BMC Biology, 13: 82. https://doi.org/10.1186/s12915-015-0192-7
 
Lattanzio, M.S. and Miles, D.B. 2016. Trophic niche divergence among colour morphs that exhibit alternative mating tactics. Royal Society Open Science. 3: 150531. https://doi.org/10.1098/rsos.150531
 
Scali, S., Sacchi, R., Mangiacotti, M., Pupin, F., Gentilli, A., Zucchi, C. Scannolo, M., Pavesi, M., Zuffi, M.A.L. 2016. Does a polymorphic species have a ‘polymorphic’ diet? A case study from a lacertid lizard. Biologcial Journal of the Linnean Society. 117: 492-502. https://doi.org/10.1111/bij.12652

de Solan T, Sinervo B, Geniez P, David P, Crochet P-A (2023) Colour polymorphism and conspicuousness do not increase speciation rates in Lacertids. bioRxiv, 2023.02.15.528678, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.02.15.528678

West-Eberhard, M.J. 1986. Alternative adaptations, speciation, and phylogeny (A review). Proceedings of the National Academy of Sciences. 83: 1388-1392. https://doi.org/10.1073/pnas.83.5.1388
 
Whitney, J.L., Donahue, M.J., Karl, S.A. 2018. Niche divergence along a fine-scale ecological gradient in sympatric colour morphs of a coral reef fish. Ecosphere. 9: e02015. https://doi.org/10.1002/ecs2.2015