Starting with the seminar paper by Lande & Arnold (1983), several studies have addressed phenotypic selection in natural populations of a wide variety of organisms, with a recent renewed interest in forest trees (e.g., Oddou-Muratorio et al. 2018; Alexandre et al. 2020; Westergren et al. 2023). Because of their long generation times, long-lived organisms such as forest trees may suffer the most from maladaptation due to climate change, and whether they will be able to adapt to new environmental conditions in just one or a few generations is hotly debated.

In this study, Oddou-Muratorio and colleagues (2024) extend the current framework to add two additional selection components that may alter patterns of fecundity selection and the estimation of standard selection gradients, namely sexual selection (evaluated as differences in flowering phenology conducting to assortative mating) and growth (viability) selection. Notably, the study is conducted in two contrasted environments (low vs high altitude populations) providing information on how the environment may modulate selection patterns in spring phenology. Spring phenology is a key adaptive trait that has been shown to be already affected by climate change in forest trees (Alberto et al. 2013). While fecundity selection for early phenology has been extensively reported before (see Munguía-Rosas et al. 2011), the authors found that this kind of selection can be strongly modulated by sexual selection, depending on the environment. Moreover, they found a significant correlation between early phenology and seedling growth in a common garden, highlighting the importance of this trait for early survival in European beech.

As a conclusion, this original research puts in evidence the need for more integrative approaches for the study of natural selection in the field, as well as the importance of testing multiple environments and the relevance of common gardens to further evaluate phenotypic changes due to real-time selection.

PS: The recommender and the first author of the preprint have shared authorship in a recent paper in a similar topic (Westergren et al. 2023). Nevertheless, the recommender has not contributed in any way or was aware of the content of the current preprint before acting as recommender, and steps have been taken for a fair and unpartial evaluation.

References

Alberto, F. J., Aitken, S. N., Alía, R., González‐Martínez, S. C., Hänninen, H., Kremer, A., Lefèvre, F., Lenormand, T., Yeaman, S., Whetten, R., & Savolainen, O. (2013). Potential for evolutionary responses to climate change - evidence from tree populations. Global Change Biology, 19(6), 1645‑1661.
https://doi.org/10.1111/gcb.12181
 
Alexandre, H., Truffaut, L., Klein, E., Ducousso, A., Chancerel, E., Lesur, I., Dencausse, B., Louvet, J., Nepveu, G., Torres‐Ruiz, J. M., Lagane, F., Musch, B., Delzon, S., & Kremer, A. (2020). How does contemporary selection shape oak phenotypes? Evolutionary Applications, 13(10), 2772‑2790.
https://doi.org/10.1111/eva.13082
 
Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37(6), 1210-1226.
https://doi.org/10.2307/2408842
 
Munguía-Rosas, M. A., Ollerton, J., Parra-Tabla, V., & De-Nova, J. A. (2011). Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters, 14(5), 511-521
https://doi.org/10.1111/j.1461-0248.2011.01601.x

Oddou-Muratorio S, Bontemps A, Gauzere J, Klein E (2024) Interplay between fecundity, sexual and growth selection on the spring phenology of European beech (Fagus sylvatica L.). bioRxiv, 2023.04.27.538521, ver. 2 peer-reviewed and recommended by Peer Community In Evolutionary Biology https://doi.org/10.1101/2023.04.27.538521 

Oddou-Muratorio, S., Gauzere, J., Bontemps, A., Rey, J.-F., & Klein, E. K. (2018). Tree, sex and size: Ecological determinants of male vs. female fecundity in three Fagus sylvatica stands. Molecular Ecology, 27(15), 3131‑3145.
https://doi.org/10.1111/mec.14770
 
Westergren, M., Archambeau, J., Bajc, M., Damjanić, R., Theraroz, A., Kraigher, H., Oddou‐Muratorio, S., & González‐Martínez, S.C. (2023). Low but significant evolutionary potential for growth, phenology and reproduction traits in European beech. Molecular Ecology, Early View 
https://doi.org/10.1111/mec.17196

At the very end of a paper entitled "Copepodology for the ornithologist" Hutchinson (1951) pointed out the possibility of 'fugitive species'.  A fugitive species, said Hutchinson, is one that we would typically think of as competitively inferior.  Wherever it happens to live it will eventually be overwhelmed by competition from another species.  We would expect it to rapidly go extinct but for one reason: it happens to be a much better coloniser than the other species.  Now all we need to explain its persistence is a dose of space and a little disturbance: a world in which there are occasional disturbances that cause local extinction of the dominant species. Now, argued Hutchinson, we have a recipe for persistence, albeit of a harried kind.  As Hutchinson put it, fugitive species "are forever on the move, always becoming extinct in one locality as they succumb to competition, and always surviving as they reestablish themselves in some other locality."

It is a fascinating idea, not just because it points to an interesting strategy, but also because it enriches our idea of competition: competition for space can be just as important as competition for time.

Hutchinson's idea was independently discovered with the advent of metapopulation theory (Levins 1971; Slatkin 1974) and since then, of course, ecologists have gone looking, and they have unearthed many examples of species that could be said to have a fugitive lifestyle.  These fugitive species are out there, but we don't often get to see them evolve.  

In their recent paper, Chapuis et al. (2024) make a convincing case that they have seen the evolution of a fugitive species.  They catalog the arrival of an invasive freshwater snail on Guadeloupe in the Lesser Antilles, and they wonder what impact this snail's arrival might have on a native freshwater snail.  This is a snail invasion, so it has been proceeding at a majestic pace, allowing the researchers to compare populations of the native snail that are completely naive to the invader with those that have been exposed to the invader for either a relatively short period (<20 generations) or longer periods (>20 generations).  They undertook an extensive set of competition assays on these snails to find out which species were competitively superior and how the native species' competitive ability has evolved over time.

Against naive populations of the native, the invasive snail turns out to be unequivocally the stronger competitor.  (This makes sense; it probably wouldn't have been able to invade if it wasn't.)  So what about populations of the native snail that have been exposed for longer, that have had time to adapt?  Surprisingly these populations appear to have evolved to become even weaker competitors than they already were. 

So why is it that the native species has not simply been driven extinct? Drawing on their previous work on this system, the authors can explain this situation.  The native species appears to be the better coloniser of new habitats.  Thus, it appears that the arrival of the invasive species has pushed the native species into a different place along the competition-colonisation axis.  It has sacrificed competitive ability in favour of becoming a better coloniser; it has become a fugitive species in its own backyard.

This is a really nice empirical study.  It is a large lab study, but one that makes careful sampling around a dynamic field situation.  Thus, it is a lab study that informs an earlier body of fieldwork and so reveals a fascinating story about what is happening in the field. We are left not only with a particularly compelling example of character displacement towards a colonising phenotype but also with something a little less scientific: the image of a hobo snail, forever on the run, surviving in the spaces in between.

References

Chapuis E, Jarne P, David P (2024) Rapid life-history evolution reinforces competitive asymmetry between invasive and resident species. bioRxiv, 2023.10.25.563987, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.10.25.563987

Hutchinson, G.E. (1951) Copepodology for the Ornithologist. Ecology 32: 571–77. https://doi.org/10.2307/1931746

Levins, R., and D. Culver. (1971) Regional Coexistence of Species and Competition between Rare Species. Proceedings of the National Academy of Sciences 68, no. 6: 1246–48. https://doi.org/10.1073/pnas.68.6.1246.

Slatkin, Montgomery. (1974) Competition and Regional Coexistence. Ecology 55, no. 1: 128–34. https://doi.org/10.2307/1934625.

In this study, Ishigohoka and colleagues tackle an important, yet often overlooked, question on the causes of genetic variation. While genome-wide patterns represent population structure, local variation is often associated with selection. Authors propose that an alternative cause for variation in individual loci is reduced recombination rate.

To test this hypothesis, authors perform local Principal Component Analysis (PCA) (Li & Ralph, 2019) to identify local deviations in population structure in the Eurasian blackcap (Sylvia atricapilla) (Ishigohoka et al. 2022). This approach is typically used to detect chromosomal rearrangements or any long region of linked loci (e.g., due to reduced recombination or selection) (Mérot et al. 2021). While other studies investigated the effect of low recombination on genetic variation (Booker et al. 2020), here authors provide a comprehensive analysis of the effect of recombination to local PCA patterns both in empirical and simulated data sets. Findings demonstrate that low recombination (and not selection) can be the sole explanatory variable for outlier windows. The study also describes patterns of genetic variation along the genome of Eurasian blackcaps, localising at least two polymorphic inversions (Ishigohoka et al. 2022).

Further investigations on the effect of model parameters (e.g., window sizes and thresholds for defining low-recombining regions), as well as the use of powerful neutrality tests are in need to clearly assess whether outlier regions experience selection and reduced recombination, and to what extent.

References

Booker, T. R., Yeaman, S., & Whitlock, M. C. (2020). Variation in recombination rate affects detection of outliers in genome scans under neutrality. Molecular Ecology, 29 (22), 4274–4279. https://doi.org/10.1111/mec.15501

Ishigohoka, J., Bascón-Cardozo, K., Bours, A., Fuß, J., Rhie, A., Mountcastle, J., Haase, B., Chow, W., Collins, J., Howe, K., Uliano-Silva, M., Fedrigo, O., Jarvis, E. D., Pérez-Tris, J., Illera, J. C., Liedvogel, M. (2022) Distinct patterns of genetic variation at low-recombining genomic regions represent haplotype structure. bioRxiv 2021.12.22.473882, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.12.22.473882

Li, H., & Ralph, P. (2019). Local PCA Shows How the Effect of Population Structure Differs Along the Genome. Genetics, 211 (1), 289–304. https://doi.org/10.1534/genetics.118.301747

Mérot, C., Berdan, E. L., Cayuela, H., Djambazian, H., Ferchaud, A.-L., Laporte, M., Normandeau, E., Ragoussis, J., Wellenreuther, M., & Bernatchez, L. (2021). Locally Adaptive Inversions Modulate Genetic Variation at Different Geographic Scales in a Seaweed Fly. Molecular Biology and Evolution, 38 (9), 3953–3971. https://doi.org/10.1093/molbev/msab143

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