Biodiversity is unevenly distributed over time, space and the tree of life [1]. The fact that regions are richer than others as exemplified by the latitudinal diversity gradient has fascinated biologists as early as the first explorers travelled around the world [2]. Provincialism was one of the first general features of land biotic distributions noted by famous nineteenth century biologists like the phytogeographers J.D. Hooker and A. de Candolle, and the zoogeographers P.L. Sclater and A.R. Wallace [3]. When these explorers travelled among different places, they were struck by the differences in their biotas (e.g. [4]). The limited distributions of distinctive endemic forms suggested a history of local origin and constrained dispersal. Much biogeographic research has been devoted to identifying areas where groups of organisms originated and began their initial diversification [3]. Complementary efforts found evidence of both historical barriers that blocked the exchange of organisms between adjacent regions and historical corridors that allowed dispersal between currently isolated regions. The result has been a division of the Earth into a hierarchy of regions reflecting patterns of faunal and floral similarities (e.g. regions, subregions, provinces). Therefore a first ensuing question is: “how regional species pools have been assembled through time and space?”, which can be followed by a second question: “what are the ecological and evolutionary processes leading to differences in species richness among species pools?”.

To address these questions, the study of Calatayud et al. [5] developed and performed an interesting approach relying on phylogenetic data to identify regional and sub-regional pools of European beetles (using the iconic ground beetle genus Carabus). Specifically, they analysed the processes responsible for the assembly of species pools, by comparing the effects of dispersal barriers, niche similarities and phylogenetic history. They found that Europe could be divided in seven modules that group zoogeographically distinct regions with their associated faunas, and identified a transition zone matching the limit of the ice sheets at Last Glacial Maximum (19k years ago). Deviance of species co-occurrences across regions, across sub-regions and within each region was significantly explained, primarily by environmental niche similarity, and secondarily by spatial connectivity, except for northern regions. Interestingly, southern species pools are mostly separated by dispersal barriers, whereas northern species pools are mainly sorted by their environmental niches. Another important finding of Calatayud et al. [5] is that most phylogenetic structuration occurred during the Pleistocene, and they show how extreme recent historical events (Quaternary glaciations) can profoundly modify the composition and structure of geographic species pools, as opposed to studies showing the role of deep-time evolutionary processes.

The study of biogeographic assembly of species pools using phylogenies has never been more exciting and promising than today. Catalayud et al. [5] brings a nice study on the importance of Pleistocene glaciations along with geographical barriers and niche-based processes in structuring the regional faunas of European beetles. The successful development of powerful analytical tools in recent years, in conjunction with the rapid and massive increase in the availability of biological data (including molecular phylogenies, fossils, georeferrenced occurrences and ecological traits), will allow us to disentangle complex evolutionary histories. Although we still face important limitations in data availability and methodological shortcomings, the last decade has witnessed an improvement of our understanding of how historical and biotic triggers are intertwined on shaping the Earth’s stupendous biological diversity. I hope that the Catalayud et al.’s approach (and analytical framework) will help movement in that direction, and that it will provide interesting perspectives for future investigations of other regions. Applied to a European beetle radiation, they were able to tease apart the relative contributions of biotic (niche-based processes) versus abiotic (geographic barriers and climate change) factors.

References

[1] Rosenzweig ML. 1995. Species diversity in space and time. Cambridge: Cambridge University Press.
[2] Mittelbach GG, Schemske DW, Cornell HV, Allen AP, Brown JM et al. 2007. Evolution and the latitudinal diversity gradient: speciation, extinction and biogeography. Ecology Letters. 10: 315–331. doi: 10.1111/j.1461-0248.2007.01020.x
[3] Lomolino MV, Riddle BR, Whittaker RJ and Brown JH. 2010. Biogeography, 4th edn. Sinauer Associates, Inc., Sunderland, MA.
[4] Wallace AR. 1876. The geographical distribution of animals: with a study of the relations of living and extinct faunas as elucidating the past changes of the earth's surface. New York: Harper and Brothers, Publishers.
[5] Calatayud J, Rodríguez MÁ, Molina-Venegas R, Leo M, Hórreo JL and Hortal J. 2018. Pleistocene climate change and the formation of regional species pools. bioRxiv 149617 ver. 4 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/149617

Studies in speciation genomics have revealed that gene flow is quite common, and that despite this, species can maintain their distinct environmental adaptations. Although researchers are still elucidating the genomic mechanisms by which species maintain their adaptations in the face of gene flow, this often appears to involve few diverged genomic regions in otherwise largely undifferentiated genomes. In this preprint [1], Riquet and colleagues investigate the genetic structuring and patterns of parallel evolution in the long-snouted seahorse.
Before investigating specific SNPs plausibly associated with adaptation, the authors first describe genome-wide population structure in the long-snouted seahorse. This species is split into five phenotypically similar, but genetically distinct populations. Two populations reside in the Atlantic Ocean and are geographically structured with one north of the Iberian peninsula and the other around the Iberian peninsula. Two other populations are found in the Mediterranean Sea and are structured by the environment as they correspond to marine and lagoon environments. The genetic clustering of lagoon populations in the Mediterranean, despite the substantial geographic distance between them is quite impressive, and worthy of further study. Finally, a fifth population resides in a lagoon-like habitat in the Black Sea.
The authors then investigate patterns of extreme genomic differentiation among populations, and uncover a remarkable pattern of parallel differentiation in these populations. In an outlier scan, Riquet and colleagues find numerous SNPs in one genomic region that separates northern and southern Atlantic populations. Quiet surprisingly, this same genomic region appears to differentiate populations living in marine and lagoon habitats in the Mediterranean. The idea that parallel patterns of genomic differentiation may underlie adaptation to differing environmental scenarios has not yet received much attention. This paper should change that. This paper is particularity impressive in that the authors uncovered this intriguing pattern with under three hundred SNPs. Future genome scale studies will uncover the genomic basis behind this unusual case of parallelism.

References

[1] Riquet, F., Liautard-Haag, C., Woodall, L., Bouza, C., Louisy, P., Hamer, B., Otero-Ferrer, F., Aublanc, P., Béduneau, V., Briard, O., El Ayari, T., Hochscheid, S. Belkhir, K., Arnaud-Haond, S., Gagnaire, P.-A., Bierne, N. (2018). Parallel pattern of differentiation at a genomic island shared between clinal and mosaic hybrid zones in a complex of cryptic seahorse lineages. bioRxiv, 161786, ver. 4 recommended and peer-reviewed by PCI Evol Biol. doi: 10.1101/161786

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

Monnin et al. [1] here studied how Drosophila populations are affected when exposed to a high virulent endosymbiotic wMelPop Wolbachia strain and why virulent vertically transmitting endosymbionts persist in nature. This virulent wMelPop strain has been described to be a blocker of dengue and other arboviral infections in arthropod vector species, such as Aedes aegypti. Whereas it can thus function as a mutualistic symbiont, it here acts as an antagonist along the mutualism-antagonism continuum symbionts operate. The wMelPop strain is not a natural occurring strain in Drosophila melanogaster and thus the start of this experiment can be seen as a novel host-pathogen association. Through experimental evolution of 17 generations, the authors studied how high temperature affects wMelPop Wolbachia virulence and Drosophila melanogaster survival. The authors used Drosophila strains that were selected for late reproduction, given that this should favor evolution to a lower virulence. Assumptions for this hypothesis are not given in the manuscript here, but it can indeed be assumed that energy that is assimilated to symbiont tolerance instead of reproduction may lead to reduced virulence evolution. This has equally been suggested by Reyserhove et al. [2] in a dynamics energy budget model tailored to Daphnia magna virulence evolution upon a viral infection causing White fat Cell disease, reconstructing changing environments through time.
Contrary to their expectations for vertically transmitting symbionts, the authors did not find a reduction in wMelPop Wolbachia virulence during the course of the experimental evolution experiment under high temperature. Important is what this learns for virulence evolution, also for currently horizontal transmitting disease epidemics (such as COVID-19). It mainly reflects that evolution of virulence for new host-pathogen associations is difficult to predict and that it may take multiple generations before optimal levels of virulence are reached [3,4]. These optimal levels of virulence will depend on trade-offs with other life history traits of the symbiont, but also on host demography, host heterogeneity, amongst others [5,6]. Multiple microbial interactions may affect the outcome of virulence evolution [7]. Given that no germ-free individuals were used, it can be expected that other components of the Drosophila microbiome may have played a role in the virulence evolution. In most cases, microbiota have been described as defensive or protective for virulent symbionts [8], but they may also have stimulated the high levels of virulence. Especially, given that upon higher temperatures, Wolbachia growth may have been increased, host metabolic demands increased [9], host immune responses affected and microbial communities changed [10]. This may have resulted in increased competitive interactions to retrieve host resources, sustaining high virulence levels of the symbiont.
A nice asset of this study is that the phenotypic results obtained in the experimental evolution set-up were linked with wMelPop density measurement and octomom copy number quantifications. Octomom is a specific 8-n genes region of the Wolbachia genome responsible for wMelPop virulence, so there is a link between the phenotypic and molecular functions of the involved symbiont. The authors found that density, octomom copy number and virulence were correlated to each other. An important note the authors address in their discussion is that, to exclude the possibility that octomom copy number has an effect on density, and density on virulence, the effect of these variables should be assessed independently of temperature and age. The obtained results are a valuable contribution to the ongoing debate on the relationship between wMelPop octomom copy number, density and virulence.

References

[1] Monnin, D., Kremer, N., Michaud, C., Villa, M., Henri, H., Desouhant, E. and Vavre, F. (2020) Experimental evolution of virulence and associated traits in a Drosophila melanogaster – Wolbachia symbiosis. bioRxiv, 2020.04.26.062265, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: https://doi.org/10.1101/2020.04.26.062265
[2] Reyserhove, L., Samaey, G., Muylaert, K., Coppé, V., Van Colen, W., and Decaestecker, E. (2017). A historical perspective of nutrient change impact on an infectious disease in Daphnia. Ecology, 98(11), 2784-2798. doi: https://doi.org/10.1002/ecy.1994
[3] Ebert, D., and Bull, J. J. (2003). Challenging the trade-off model for the evolution of virulence: is virulence management feasible?. Trends in microbiology, 11(1), 15-20. doi: https://doi.org/10.1016/S0966-842X(02)00003-3
[4] Houwenhuyse, S., Macke, E., Reyserhove, L., Bulteel, L., and Decaestecker, E. (2018). Back to the future in a petri dish: Origin and impact of resurrected microbes in natural populations. Evolutionary Applications, 11(1), 29-41. doi: https://doi.org/10.1111/eva.12538
[5] Day, T., and Gandon, S. (2007). Applying population‐genetic models in theoretical evolutionary epidemiology. Ecology Letters, 10(10), 876-888. doi: https://doi.org/10.1111/j.1461-0248.2007.01091.x
[6] Alizon, S., Hurford, A., Mideo, N., and Van Baalen, M. (2009). Virulence evolution and the trade‐off hypothesis: history, current state of affairs and the future. Journal of evolutionary biology, 22(2), 245-259. doi: https://doi.org/10.1111/j.1420-9101.2008.01658.x
[7] Alizon, S., de Roode, J. C., and Michalakis, Y. (2013). Multiple infections and the evolution of virulence. Ecology letters, 16(4), 556-567. doi: https://doi.org/10.1111/ele.12076
[8] Decaestecker, E., and King, K. (2019). Red queen dynamics. Reference module in earth systems and environmental sciences, 3, 185-192. doi: https://doi.org/10.1016/B978-0-12-409548-9.10550-0
[9] Kirk, D., Jones, N., Peacock, S., Phillips, J., Molnár, P. K., Krkošek, M., and Luijckx, P. (2018). Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics. PLoS biology, 16(2), e2004608. doi: https://doi.org/10.1371/journal.pbio.2004608
[10] Frankel-Bricker, J., Song, M. J., Benner, M. J., and Schaack, S. (2019). Variation in the microbiota associated with Daphnia magna across genotypes, populations, and temperature. Microbial ecology, 1-12. doi: https://doi.org/10.1007/s00248-019-01412-9

Biological invasions are natural experiments, and often show that evolution can affect dynamics in important ways [1-3]. While we often think of invasions as a conservation problem stemming from anthropogenic introductions [4,5], biological invasions are much more commonplace than this, including phenomena as diverse as natural range shifts, the spread of novel pathogens, and the growth of tumors. A major question across all these settings is which set of traits determine the ability of a population to invade new space [6,7]. Traits such as: increased growth or reproductive rate, dispersal ability and ability to defend from predation often show large evolutionary shifts across invasion history [1,6,8]. Are such multi-trait shifts driven by selection on multiple traits, or a correlated response by multiple traits to selection on one? Resolving this question is important for both theoretical and practical reasons [9,10]. But despite the importance of this issue, it is not easy to perform the necessary manipulative experiments [9].
Foucaud et al. [11] tackled this issue by performing experimental evolution on source populations of the invasive ladybug Harmonia axyridis. The authors tested if selection on a single trait could generate correlated responses in other life history traits. Specifically, they used experimental evolution to impose divergent selection on female mass, and reproductive timing. After ten generations, they found that selection for weight did not affect almost any other life history trait. However, nine generations of selection for faster reproduction led to correlated phenotypic changes in developmental, reproduction and survival rate of populations, although not always in the direction we might have expected. Despite this correlated response, none of their selected lines were able to fully recapitulate the trait shifts seen in natural invasions of this species. This implies that selection during natural invasions is operating on multiple traits; a finding in agreement with our growing understanding of how selection acts during introduction and invasion [12,13].
Populations undergoing a colonization process may also be subject to a multitude of different selective pressures [14,15]. The authors expanded their work in this direction by testing whether food availability alters the observed correlations between life history traits. The pervasiveness of genotype by environment interactions observed also points to a role for multiple selective pressures in shaping the suite of life-history shifts observed in wild ladybug populations. The work from Foucaud and colleagues [11] adds to a small but growing list of important studies that use experimental evolution to investigate how life-history traits evolve, and how they evolve during invasions in particular.

References

[1] Sakai, A.K., Allendorf, F.W., Holt, J.S. et al. (2001). The population biology of invasive species. Annual review of ecology and systematics, 32(1), 305-332. doi: 10.1146/annurev.ecolsys.32.081501.114037
[2] Hairston Jr, N. G., Ellner, S. P., Geber, M. A., Yoshida, T. and Fox, J. A. (2005). Rapid evolution and the convergence of ecological and evolutionary time. Ecology letters, 8(10), 1114-1127. doi: 10.1111/j.1461-0248.2005.00812.x
[3] Chuang, A. and Peterson, C. R. (2016). Expanding population edges: theories, traits, and trade‐offs. Global change biology, 22(2), 494-512. doi: 10.1111/gcb.13107
[4] Whitney, K. D. and Gabler, C. A. (2008). Rapid evolution in introduced species,‘invasive traits’ and recipient communities: challenges for predicting invasive potential. Diversity and Distributions, 14(4), 569-580. doi: 10.1111/j.1472-4642.2008.00473.x
[5] Catullo, R. A., Llewelyn, J., Phillips, B. L. and Moritz, C. C. (2019). The Potential for Rapid Evolution under Anthropogenic Climate Change. Current Biology, 29(19), R996-R1007. doi: 10.1016/j.cub.2019.08.028
[6] Suarez, A. V. and Tsutsui, N. D. (2008). The evolutionary consequences of biological invasions. Molecular Ecology, 17(1), 351-360. doi: 10.1111/j.1365-294X.2007.03456.x
[7] Deforet, M., Carmona-Fontaine, C., Korolev, K. S. and Xavier, J. B. (2019). Evolution at the edge of expanding populations. The American Naturalist, 194(3), 291-305. doi: 10.1086/704594
[8] Phillips, B. L., Brown, G. P., and Shine, R. (2010). Life‐history evolution in range‐shifting populations. Ecology, 91(6), 1617-1627. doi: 10.1890/09-0910.1
[9] Colautti, R. I. and Lau, J. A. (2015). Contemporary evolution during invasion: evidence for differentiation, natural selection, and local adaptation. Molecular ecology, 24(9), 1999-2017. doi: 10.1111/mec.13162
[10] Szűcs, M., Melbourne, B. A., Tuff, T., Weiss‐Lehman, C. and Hufbauer, R. A. (2017). Genetic and demographic founder effects have long‐term fitness consequences for colonising populations. Ecology Letters, 20(4), 436-444. doi: 10.1111/ele.12743
[11] Foucaud, J., Hufbauer, R. A., Ravigné, V., Olazcuaga, L., Loiseau, A., Ausset, A., Wang, S., Zang, L.-S., Lemenager, N., Tayeh, A., Weyna, A., Gneux, P., Bonnet, E., Dreuilhe, V., Poutout, B., Estoup, A. and Facon, B. (2020). How do invasion syndromes evolve? An experimental evolution approach using the ladybird Harmonia axyridis. bioRxiv, 849968 ver. 4 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/849968
[12] Simons, A. M. (2003). Invasive aliens and sampling bias. Ecology Letters, 6(4), 278-280. doi: 10.1046/j.1461-0248.2003.00430.x
[13] Phillips, B. L. and Perkins, T. A. (2019). Spatial sorting as the spatial analogue of natural selection. Theoretical Ecology, 12(2), 155-163. doi: 10.1007/s12080-019-0412-9
[14] Lavergne, S. and Molofsky, J. (2007). Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proceedings of the National Academy of Sciences, 104(10), 3883-3888. doi: 10.1073/pnas.0607324104
[15] Moran, E. V. and Alexander, J. M. (2014). Evolutionary responses to global change: lessons from invasive species. Ecology Letters, 17(5), 637-649. doi: 10.1111/ele.12262