Sex chromosomes evolve as recombination is suppressed between the X and Y chromosomes. The loss of recombination on the sex-limited chromosome (the Y in mammals) leads to degeneration of both gene expression and gene content for many genes [1]. Loss of gene expression or content from the Y chromosome leads to differences in gene dose between males and females for X-linked genes. Because expression levels are often correlated with gene dose [2], these hemizygous genes have a lower expression levels in the heterogametic sex. This in turn disrupts the stoichiometric balance among genes in protein complexes that have components on both the sex chromosomes and autosomes [3], which could have serious deleterious consequences for the heterogametic sex.
To overcome these deleterious effects of degeneration, the expression levels of dosage sensitive X-linked genes, and in some organisms, entire X chromosomes, are compensated, the expression of the single copy of in the heterogametic sex being increased. Dosage compensation for such genes has evolved in several species, restoring similar expression levels as in the ancestral state in males and/or equal gene expression in males and females [4-8]. The mechanisms for dosage compensation are variable among species and their evolutionary paths are not fully understood, as the few model sex chromosomes studied so far have old, and highly degenerate sex chromosomes [4-7].
Muyle et al. [9] studied the young sex chromosomes of the plant Silene latifolia, which has young sex chromosomes (4 MY) and highly variable dosage compensation [10, 11]. The authors used both an outgroup species without sex chromosomes for obtaining a proxy for ancestral expression levels before Y degeneration, and implemented methods to identify sex-linked genes and disentangle paternal versus maternal allele expression [12]. Using these elements, Muyle et al. [9] reveal upregulation of maternal X alleles in both males and females in the young S. latifolia sex chromosomes [9], possibly by genomic imprinting. The upregulation in both sexes of the maternal X alleles likely yields non-optimal gene expression in females, which is strikingly consistent with the theoretical first step of dosage compensation as postulated by Ohno [8], which predicts restoration of ancestral expression in males, over-expression in females, and unequal expression in the two sexes. These findings provide surprising insight into the earliest stages of dosage compensation, one of the most intriguing aspects of evolutionary biology.

References
[1] Bachtrog D. 2013. Y chromosome evolution: emerging insights into processes of Y-chromosome degeneration? Nature Reviews Genetics 14: 113–124. doi: 10.1038/nrg3366
[2] Malone JH, Cho D-Y, Mattiuzzo NR, Artieri CG, Jiang L, Dale RK, Smith HE, McDaniel J, Munro S, Salit M, Andrews J, Przytycka TM and Oliver B. 2012. Mediation of Drosophila autosomal dosage effects and compensation by network interactions. Genome Biology 13: R28. doi: 10.1186/gb-2012-13-4-r28
[3] Pessia E, Makino T, Bailly-Bechet M, McLysaght A and Marais GAB. 2012. Mammalian X chromosome inactivation evolved as a dosage-compensation mechanism for dosage-sensitive genes on the X chromosome. Proceedings of the National Academy of Sciences of the United States of America. 109: 5346–5351. doi: 10.1073/pnas.1116763109.
[4] Graves JAM. 2016. Evolution of vertebrate sex chromosomes and dosage compensation. Nature Reviews Genetics 17: 33–46. doi: 10.1038/nrg.2015.2
[5] Mank JE. 2013. Sex chromosome dosage compensation: definitely not for everyone. Trends in Genetics 12: 677–683. doi: 10.1016/j.tig.2013.07.005
[6] Pessia E and Engelstädter J. 2014. The evolution of X chromosome inactivation in mammals: the demise of Ohno’s hypothesis? Cellular and Molecular Life Sciences 71: 1383–1394. doi: 10.1007/s00018-013-1499-6
[7] Muyle A, Shearn R and Marais GAB. 2017. The evolution of sex chromosomes and dosage compensation in plants. Genome Biology and Evolution 9: 627–645. doi: 10.1093/gbe/evw282
[8] Ohno S. 1967. Sex chromosomes and sex linked genes. Springer, Berlin Heidelberg New York.
[9] Muyle A, Zemp N, Fruchard C, Cegan R, Vrana J, Deschamps C, Tavares R, Picard F, Hobza R, Widmer A and Marais GAB. 2018. Genomic imprinting mediates dosage compensation in a young plant XY system. bioRxiv 118695, ver. 6 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/179044
[10] Papadopulos AST, Chester M, Ridout K and Filatov DA. 2015. Rapid Y degeneration and dosage compensation in plant sex chromosomes. Proceedings of the National Academy of Sciences of the United States of America 112: 13021–13026. doi: 10.1073/pnas.1508454112
[11] Bergero R, Qiu S and Charlesworth D. 2015. Gene loss from a plant sex chromosome system. Current Biology 25: 1234–1240. doi: 10.1016/j.cub.2015.03.015
[12] Muyle A, Kafer J, Zemp N, Mousset S, Picard F and Marais GAB. 2016. SEX-DETector: a probabilistic approach to study sex chromosomes in non-model organisms. Genome Biology and Evolution 8: 2530–2543. doi: 10.1093/gbe/evw172

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

Species everywhere are facing rapid climatic change, and we are increasingly asking whether populations will adapt, shift, or perish [1]. There is a growing realisation that, despite limited within-population genetic variation, many species exhibit substantial geographic variation in climate-relevant traits. This geographic variation might play an important role in facilitating adaptation to climate change [2,3].
Much of our understanding of geographic variation in climate-relevant traits comes from model organisms [e.g. 4]. But as our concern grows, we make larger efforts to understand geographic variation in non-model organisms also. If we understand what adaptive geographic variation exists within a species, we can make management decisions around targeted gene flow [5]. And as empirical examples accumulate, we can look for generalities that can inform management of unstudied species [e.g. 6,7]. Rudin-Bitterli’s paper [8] is an excellent contribution in this direction.
Rudin-Bitterli and her co-authors [8] sampled six frog populations distributed across a strong rainfall gradient. They then assayed these frogs and their offspring for a battery of fitness-relevant traits. The results clearly show patterns consistent with local adaptation to water availability, but they also reveal trade-offs. In their study, frogs from the driest source populations were resilient to the hydric environment: it didn’t really affect them very much whether they were raised in wet or dry environments. By contrast, frogs from wet source areas did better in wet environments, and they tended to do better in these wet environments than did animals from the dry-adapted populations. Thus, it appears that the resilience of the dry-adapted populations comes at a cost: frogs from these populations cannot ramp up performance in response to ideal (wet) conditions.
These data have been carefully and painstakingly collected, and they are important. They reveal not only important geographic variation in response to hydric stress (in a vertebrate), but they also adumbrate a more general trade-off: that the jack of all trades might be master of none. Specialist-generalist trade-offs are often argued (and regularly observed) to exist [e.g. 9,10], and here we see them arise in climate-relevant traits also. Thus, Rudin-Bitterli’s paper is an important piece of the empirical puzzle, and one that points to generalities important for both theory and management.

References

[1] Hoffmann, A. A., and Sgrò, C. M. (2011). Climate change and evolutionary adaptation. Nature, 470(7335), 479–485. doi: 10.1038/nature09670
[2] Aitken, S. N., and Whitlock, M. C. (2013). Assisted Gene Flow to Facilitate Local Adaptation to Climate Change. Annual Review of Ecology, Evolution, and Systematics, 44(1), 367–388. doi: 10.1146/annurev-ecolsys-110512-135747
[3] Kelly, E., and Phillips, B. L. (2016). Targeted gene flow for conservation. Conservation Biology, 30(2), 259–267. doi: 10.1111/cobi.12623
[4] Sgrò, C. M., Overgaard, J., Kristensen, T. N., Mitchell, K. A., Cockerell, F. E., and Hoffmann, A. A. (2010). A comprehensive assessment of geographic variation in heat tolerance and hardening capacity in populations of Drosophila melanogaster from eastern Australia. Journal of Evolutionary Biology, 23(11), 2484–2493. doi: 10.1111/j.1420-9101.2010.02110.x
[5] Macdonald, S. L., Llewelyn, J., and Phillips, B. L. (2018). Using connectivity to identify climatic drivers of local adaptation. Ecology Letters, 21(2), 207–216. doi: 10.1111/ele.12883
[6] Hoffmann, A. A., Chown, S. L., and Clusella‐Trullas, S. (2012). Upper thermal limits in terrestrial ectotherms: how constrained are they? Functional Ecology, 27(4), 934–949. doi: 10.1111/j.1365-2435.2012.02036.x
[7] Araújo, M. B., Ferri‐Yáñez, F., Bozinovic, F., Marquet, P. A., Valladares, F., and Chown, S. L. (2013). Heat freezes niche evolution. Ecology Letters, 16(9), 1206–1219. doi: 10.1111/ele.12155
[8] Rudin-Bitterli, T. S., Evans, J. P., and Mitchell, N. J. (2019). Geographic variation in adult and embryonic desiccation tolerance in a terrestrial-breeding frog. BioRxiv, 314351, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. doi: 10.1101/314351
[9] Kassen, R. (2002). The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology, 15(2), 173–190. doi: 10.1046/j.1420-9101.2002.00377.x
[10] Angilletta, M. J. J. (2009). Thermal Adaptation: A theoretical and empirical synthesis. Oxford University Press, Oxford.

In evolutionary biology, sexual selection is hypothesized to increase speciation rates in animals, as theory predicts that sexual selection will contribute to phenotypic diversification and affect rates of species accumulation at macro-evolutionary time scales. However, testing this hypothesis and gathering convincing evidence have proven difficult. Although some studies have shown a strong correlation between proxies of sexual selection and species diversity (mostly in birds), this relationship relies on some assumptions on the link between these proxies and the strength of sexual selection and is not detected in some other taxa, making taxonomically widespread conclusions impossible.

In a recent study published in Current Biology [1], Ellis and Oakley provide strong evidence that bioluminescent sexual displays have driven high species richness in taxonomically diverse animal lineages, providing a crucial link between sexual selection and speciation.
It was known that bioluminescence has evolved independently more than 40 times, with males often using it as a mating signal but with also some other possible adaptive functions including anti-predator defense and predation. Moreover, it has been reported that small marine lanternfishes and sharks that use bioluminescence in mate identification had a greater concentration of species than other deep-sea fishes that use bioluminescence for defensive purposes [2-4]. But no one had ever determined whether this pattern is consistent across diverse and distantly related animal groups living on sea and land.

Ellis and Oakley [1] explored the scientific literature for well-resolved evolutionary trees with branches containing bioluminescent lineages and identified lineages that use light for courtship or camouflage in a wide range of marine and terrestrial taxa including insects, crustaceans, cephalopods, segmented worms, and fishes. The researchers counted the number of species in each bioluminescent clade and found that all groups with light-courtship displays had more species and faster rates of species accumulation than their non-luminous most closely related sister lineages or ancestors. In contrast, those groups that used bioluminescence for predator avoidance had a lower than expected rate of species richness on average.

Nicely encompassing a diversity of taxa and neatly controlling for the rate of species accumulation of the encompassing clade, the results of Ellis and Oakley are clear-cut and provide the most comprehensive evidence to date for the hypothesis that sexual displays can act as drivers of speciation. One question this study incites is what is happening in terms of sexual selection in species displaying defensive bioluminescence or no bioluminescence at all: do those lineages use no mating signals at all or other mating signals that are less apparent, and will those experience lower levels of sexual selection than bioluminescent mating signals, i.e. consistent with Ellis and Oakley results? It would also be interesting to investigate the diversification rates in animal species using other modalities, such as chemical, acoustic or any other type of signals used by males, females or both sexes, to determine what types of sexual signals may be more generally drivers of speciation.

References

[1] Ellis EA, Oakley TH. 2016. High Rates of Species Accumulation in Animals with Bioluminescent Courtship Displays. Current Biology 26:1916–1921. doi: 10.1016/j.cub.2016.05.043

[2] Davis MP, Holcroft NI, Wiley EO, Sparks JS, Smith WL. 2014. Species-specific bioluminescence facilitates speciation in the deep sea. Marine Biology 161:1139­1148. doi: 10.1007/s00227-014-2406-x

[3] Davis MP, Sparks JS, Smith WL. 2016. Repeated and Widespread Evolution of Bioluminescence in Marine Fishes. PLoS One 11:e0155154. doi: 10.1371/journal.pone.0155154

[4] Claes JM, Nilsson D-E, Mallefet J, Straube N. 2015. The presence of lateral photophores correlates with increased speciation in deep-sea bioluminescent sharks. Royal Society Open Science 2:150219. doi: 10.1098/rsos.150219

Interactions between species are a driving force in evolution. Many organisms host symbiotic partners that live all or part of their life in or on their host. Whether they are mutualistic or parasitic, these symbiotic associations impose strong selective pressures on both partners and affect their evolutionary trajectories. In fine, they can have a significant impact on the diversification patterns of both host and symbiont lineages, with symbiotic lineages sometimes speciating simultaneously with their hosts and/or switching from one host species to another. Long-term associations between species can also result in gene transfers between the involved organisms. Those lateral gene transfers are a source of ecological innovation but can obscure the phylogenetic signals and render the process of phylogenetic reconstructions complex (Lerat et al. 2003).

Methods known as reconciliations explore similarities and differences between phylogenetic trees. They have been widely used to both compare the diversification patterns of hosts and symbionts and identify lateral gene transfers between species. Though the reconciliation approaches used in host/ symbiont and species/ gene phylogenetic studies are identical, they are always applied separately to solve either molecular evolution questions or investigate the evolution of ecological interactions. However, the two questions are often intimately linked and the current interest in multi-level systems (e.g. the holobiont concept) calls for a unique model that will take into account three-level nested organization (gene/symbiont/ host) where both symbiont and genes can transfer among hosts. 

Here Menet and collaborators (2023) provide such a model to produce three-level reconciliations. In order to do so, they extend the two-level reconciliation model implemented in “ALE” software (Szöllősi et al. 2013), one of the most used and proven reconciliation methods. Briefly, given a symbiont gene tree, a symbiont tree and a host tree, as in previous reconciliation models, the symbiont tree is mapped onto the host tree by mixing three types of events: Duplication, Transfer or Loss (DTL), with a possibility of the symbiont evolving temporarily outside the host phylogeny (in a “ghost” host lineage). The gene tree evolves similarly inside the symbiont tree, but horizontal transfers are constrained to symbionts co-occurring within the same host. Joint reconciliation scenarios are reconstructed and DTL event rates and likelihoods are estimated according to the model. As a nice addition, the authors propose a method to infer the symbiont phylogeny through amalgamation from gene trees and a host tree.

The authors then explore the diverse possibilities offered by this method by testing it on both simulated datasets and biological datasets in order to check whether considering three nested levels is worthwhile. They convincingly show that three-level reconciliation has a better capacity to retrieve the symbiont donors and receivers of horizontal gene transfers, probably because transfers are constrained by additional elements relevant to the biological systems. Using, aphids, their obligate endosymbionts, and the symbiont genes involved in their nutritional functions, they identify horizontal gene transfers between aphid symbionts that are missed by two-level reconciliations but detected by expertise (Manzano-Marín et al. 2020). The other dataset presented here is on the human pathogen Helicobacter pylori, which history is supposed to reflect human migration. They use more than 1000 H. pylori gene families, and four populations, and use likelihood computations to compare different hypotheses on the diversification of the host.

In summary, this study is a proof-of-concept of a 3-level reconciliation, where the authors manage to convey the applicability of their framework to many biological systems. Reported complexities, confirmed by reported running times, show that the method is computationally efficient. Without a doubt, the tool presented here will be very useful to evolutionary biologists who want to investigate multi-scale cophylogenies and it will move forward the study of associations between host and symbionts when symbiont genomic data are available.

REFERENCES

Lerat, E., Daubin, V., & Moran, N. A. (2003). From gene trees to organismal phylogeny in prokaryotes: the case of the γ-Proteobacteria. PLoS biology, 1(1), e19.
https://doi.org/10.1371/journal.pbio.0000019
 
Manzano-Marın, A., Coeur d'acier, A., Clamens, A. L., Orvain, C., Cruaud, C., Barbe, V., & Jousselin, E. (2020). Serial horizontal transfer of vitamin-biosynthetic genes enables the establishment of new nutritional symbionts in aphids' di-symbiotic systems. The ISME Journal, 14(1), 259-273.
https://doi.org/10.1038/s41396-019-0533-6

Menet H, Trung AN, Daubin V, Tannier E (2023) Host-symbiont-gene phylogenetic reconciliation. bioRxiv, 2022.07.01.498457, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.07.01.498457

Szöllősi, G. J., Rosikiewicz, W., Boussau, B., Tannier, E., & Daubin, V. (2013). Efficient exploration of the space of reconciled gene trees. Systematic biology, 62(6), 901-912.
https://doi.org/10.1093/sysbio/syt054