Studying the effects of speciation, hybridisation, and evolutionary outcomes following reproduction from divergent populations is a major research area in evolutionary genetics [1]. There are two phenomena that have been the focus of contemporary research. First, a classic concept is the formation of ‘Bateson-Dobzhansky-Muller’ incompatibilities (BDMi) [2–4] that negatively affect hybrid fitness. Here, two diverging populations accumulate mutations over time that are unique to that subpopulation. If they subsequently meet, then these mutations might negatively interact, leading to a loss in fitness or even a complete lack of reproduction. BDMi formation can be complex, involving multiple genes and the fitness changes can depend on the direction of introgression [5]. Second, such secondary contact can instead lead to heterosis, where offspring are fitter than their parental progenitors [6].

Understanding which outcomes are likely to arise require one to know the potential fitness effects of mutations underlying reproductive isolation, to determine whether they are likely to reduce or enhance fitness when hybrids are formed. This is far from an easy task, as it requires one to track mutations at several loci, along with their effects, across a fitness landscape.

The work of De Sanctis et al. [7] neatly fills in this knowledge gap, by creating a general mathematical framework for describing the consequences of a cross from two divergent populations. The derivations are based on Fisher’s Geometric Model, which is widely used to quantify selection acting on a general fitness landscape that is affected by several biological traits [8,9], and has previously been used in theoretical studies of hybridisation [10–12]. By doing so, they are able to decompose how divergence at multiple loci affects offspring fitness through both additive and dominance effects.

A key result arising from their analyses is demonstrating how offspring fitness can be captured by two main functions. The first one is the ‘net effect of evolutionary change’ that, broadly defined, measures how phenotypically divergent two populations are. The second is the ‘total amount of evolutionary change’, which reflects how many mutations contribute to divergence and the effect sizes captured by each of them. The authors illustrate these measurements using simulations covering different scenarios, demonstrating how different parental states can lead to similar fitness outcomes. They also propose experimental methods to measure the underlying mutational effects.

This study neatly demonstrates how complex genetic phenomena underlying hybridisation can be captured using fairly simple mathematical formulae. This powerful approach will thus open the door for future research to investigate hybridisation in more detail, whether it is by expanding on these theoretical models or using the elegant outcomes to quantify fitness effects in experiments.

References

1. Coyne JA, Orr HA. Speciation. Sunderland, Mass: Sinauer Associates; 2004.
2. Bateson W, Seward A. Darwin and modern science. Heredity and variation in modern lights. 1909;85: 101. https://doi.org/10.1017/CBO9780511693953.007
3. Dobzhansky T. Genetics and the Origin of Species. Columbia university press; 1937.
4. Muller HJ. Isolating mechanisms, evolution and temperature. Biol Symp. 1942;6: 71-125.
5. Fraïsse C, Elderfield JAD, Welch JJ. The genetics of speciation: are complex incompatibilities easier to evolve? J Evol Biol. 2014;27: 688-699. https://doi.org/10.1111/jeb.12339
6. Birchler JA, Yao H, Chudalayandi S, Vaiman D, Veitia RA. Heterosis. The Plant Cell. 2010;22: 2105-2112. https://doi.org/10.1105/tpc.110.076133
7. De Sanctis B, Schneemann H, Welch JJ. How does the mode of evolutionary divergence affect reproductive isolation? bioRxiv. 2022. 2022.03.08.483443 version 4. https://doi.org/10.1101/2022.03.08.483443 
8. Fisher RA. The genetical theory of natural selection. Oxford: The Clarendon Press; 1930. https://doi.org/10.5962/bhl.title.27468 
9. Tenaillon O. The Utility of Fisher's Geometric Model in Evolutionary Genetics. Annu Rev Ecol Evol Syst. 2014;45: 179-201. https://doi.org/10.1146/annurev-ecolsys-120213-091846
10. Barton NH. The role of hybridization in evolution. Molecular Ecology. 2001;10: 551-568. https://doi.org/10.1046/j.1365-294x.2001.01216.x 
11. Chevin L-M, Decorzent G, Lenormand T. Niche Dimensionality and The Genetics of Ecological Speciation. Evolution. 2014;68: 1244-1256. https://doi.org/10.1111/evo.12346 
12. Fraïsse C, Gunnarsson PA, Roze D, Bierne N, Welch JJ. The genetics of speciation: Insights from Fisher's geometric model. Evolution. 2016;70: 1450-1464. https://doi.org/10.1111/evo.12968

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

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

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 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