In some taxa such as fish and arthropods, closely related species can have different mechanisms of sex determination and in particular different sex chromosomes, which implies that new sex chromosomes are constantly evolving [1]. Several models have been developed to explain this pattern but empirical data are lacking and the causes of the fast sex chromosome turn over remain mysterious [2-4]. Leclerq et al. [5] in a paper that just came out in PNAS have focused on one possible explanation: Wolbachia. This widespread intracellular symbiont of arthropods can manipulate its host reproduction in a number of ways, often by biasing the allocation of resources toward females, the transmitting sex. Perhaps the most spectacular example is seen in pillbugs, where Wolbachia commonly turns infected males into females, thus doubling its effective transmission to grandchildren. Extensive investigations on this phenomenon were initiated 30 years ago in the host species Armadillidium vulgare. The recent paper by Leclerq et al. beautifully validates an hypothesis formulated in these pioneer studies [6], namely, that a nuclear insertion of the Wolbachia genome caused the emergence of new female determining chromosome, that is, a new sex chromosome.

Many populations of A. vulgare are infected by the feminising Wolbachia strain wVulC, where the spread of the bacterium has also induced the loss of the ancestral female determining W chromosome (because feminized ZZ individuals produce females without transmitting any W). In these populations, all individuals carry two Z chromosomes, so that the bacterium is effectively the new sex-determining factor: specimens that received Wolbachia from their mother become females, while the occasional loss of Wolbachia from mothers to eggs allows the production of males. Intriguingly, studies from natural populations also report that some females are devoid both of Wolbachia and the ancestral W chromosome, suggesting the existence of new female determining nuclear factor, the hypothetical “f element”.

Leclerq et al. [5] found the f element and decrypted its origin. By sequencing the genome of a strain carrying the putative f element, they found that a nearly complete wVulC genome got inserted in the nuclear genome and that the chromosome carrying the insertion has effectively become a new W chromosome. The insertion is indeed found only in females, PCRs and pedigree analysis tell. Although the Wolbachia-derived gene(s) that became sex-determining gene(s) remain to be identified among many possible candidates, the genomic and genetic evidence are clear that this Wolbachia insertion is determining sex in this pillbug strain. Leclerq et al. [5] also found that although this insertion is quite recent, many structural changes (rearrangements, duplications) have occurred compared to the wVulC genome, which study will probably help understand which bacterial gene(s) have retained a function in the nucleus of the pillbug. Also, in the future, it will be interesting to understand how and why exactly the nuclear inserted Wolbachia rose in frequency in the pillbug population and how the cytoplasmic Wolbachia was lost, and to tease apart the roles of selection and drift in this event. We highly recommend this paper, which provides clear evidence that Wolbachia has caused sex chromosome turn over in one species, opening the conjecture that it might have done so in many others.

References

[1] Bachtrog D, Mank JE, Peichel CL, Kirkpatrick M, Otto SP, Ashman TL, Hahn MW, Kitano J, Mayrose I, Ming R, Perrin N, Ross L, Valenzuela N, Vamosi JC. 2014. Tree of Sex Consortium. Sex determination: why so many ways of doing it? PLoS Biology 12: e1001899. doi: 10.1371/journal.pbio.1001899

[2] van Doorn GS, Kirkpatrick M. 2007. Turnover of sex chromosomes induced by sexual conflict. Nature 449: 909-912. doi: 10.1038/nature06178

[3] Cordaux R, Bouchon D, Grève P. 2011. The impact of endosymbionts on the evolution of host sex-determination mechanisms. Trends in Genetics 27: 332-341. doi: 10.1016/j.tig.2011.05.002

[4] Blaser O, Neuenschwander S, Perrin N. 2014. Sex-chromosome turnovers: the hot-potato model. American Naturalist 183: 140-146. doi: 10.1086/674026

[5] Leclercq S, Thézé J, Chebbi MA, Giraud I, Moumen B, Ernenwein L, Grève P, Gilbert C, Cordaux R. 2016. Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proceeding of the National Academy of Science USA 113: 15036-15041. doi: 10.1073/pnas.1608979113

[6] Legrand JJ, Juchault P. 1984. Nouvelles données sur le déterminisme génétique et épigénétique de la monogénie chez le crustacé isopode terrestre Armadillidium vulgare Latr. Génétique Sélection Evolution 16: 57–84. doi: 10.1186/1297-9686-16-1-57

Perhaps because of its deadliness, the 2013-2016 Ebola Virus (EBOV) epidemics in West-Africa has led to unprecedented publication and sharing of full virus genome sequences. This was both rapid (90 full genomes were shared within weeks [1]) and important (more than 1500 full genomes have been released overall [2]). Furthermore, the availability of the metadata (especially GPS location) has led to depth analyses of the geographical spread of the epidemics [3].
In their work, Dellicour et al. [4] pursue earlier phylogeographical investigations in an original and yet simple approach to address questions of key public health importance. The originality of the approach is dual. First, from a technical standpoint, they capture the spread of infectious diseases in a continuous framework using a novel model that allows for rare long-distance dispersal events. Second, in a more classical discrete meta-population framework, they simulate the effect of public health interventions by pruning the phylogenetic tree and assessing how this affects key parameters. For instance, to simulate the effect of closing borders they remove subsets of the phylogeny that involved dispersal between countries and to simulate the effect of protecting a region by quarantine they remove all the leaves (i.e. the infections sampled) from this region. This phylogeny pruning is both original and simple. It is however limited because it currently assumes that policies are 100% effective and earlier modelling work on human influenza showed that long distance travel bans had to be implemented with >99% efficiency in order to slow epidemic growth from a time scale of days to weeks [5].
From a biological standpoint, Dellicour et al. [4] corroborate earlier findings that highly populated locations (>1,000,000 inhabitants) were crucial in explaining the magnitude of the epidemics but also show the importance of the transmission between the three capital cities. They also show that rare long-distance dispersing events of the virus are not key to explaining the magnitude of the epidemics (even though they assume 100% efficiency of suppressing long-distance event). Finally, thanks to their continuous model they estimate the speed of spread of the epidemics and are able to detect the effect of border closing on this speed.
Overall, this study [4], which involves state-of-the-art Bayesian inference methods of infection phylogenies using MCMC, stands out because of its effort to simulate public health interventions. It stands as an encouragement for the development of intervention models with increased realism and for even faster and larger virus sequence data sharing.

References

[1] Gire et al. 2014. Genomic surveillance elucidates Ebola virus origin and transmission during the 2014 outbreak. Science 345: 1369–1372. doi: 10.1126/science.1259657.
[2] Holmes EC, Dudas G, Rambaut A and Andersen KG. 2016. The evolution of Ebola virus: insights from the 2013-2016 epidemic. Nature 538: 193–200. doi: 10.1038/nature19790.
[3] Dudas et al. 2017. Virus genomes reveal factors that spread and sustained the Ebola epidemic. Nature 544: 309–315 (2017). doi: 10.1038/nature22040.
[4] Dellicour S, Baele G, Dudas G, Faria NR, Pybus OG, Suchard MA, Rambaud A and Lemey P. 2018. Phylodynamic assessment of intervention strategies for the West African Ebola virus outbreak. bioRxiv, 163691, ver. 3 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/163691.
[5] Hollingsworth TD, Ferguson NM and Anderson RM. 2006. Will travel restrictions control the international spread of pandemic influenza? Nature Medicine 12, 497–499. doi: 10.1038/nm0506-497.

The introduction of Ludwigia species as ornamental plants in both North America and Europe dates back almost two centuries, during which time they expanded as naturalized and later invasive species in these territories (Dandelot et al. 2005, Okada et al. 2009). Repeated deliberate or non-deliberate introductions over time of this species complex that can hybridize has given rise to an evolutionarily complex scenario, which is compounded by the difficulty in delimiting some of these species and by the diversity of their modes of reproduction.

Dandelot (2004) and Dandelot et al. (2005) determined the presence of two Ludwigia taxa in France, L. peploides subsp. montevidensis (Spreng.) P.H.Raven (here after Lpm), and L. grandiflora subsp. hexapetala (Hook. & Arn.) G.L.Nesom & Kartesz (here after Lgh), based on their cytotypes (2n = 16, and 2n = 80, respectively) and without evidence of hybridization between them. Furthermore, despite a predominantly vegetative reproduction observed for both species, they differed in their breeding systems. While Lpm is self-compatible and produce a high number of viable seeds in all populations, Lgh is self-incompatible and its populations may drastically differ in seed viability (Dandelot 2004). Several years later, Portillo-Lemus et al. (2021) determined that the differences in seed production between some populations of Lgh are due to the existence of a heteromorphic reproductive system in this taxon, involving a self-incompatible morph (long-style morph; hereafter L-morph), and a self-compatible morph (short-style morph: hereafter S-morph). Moreover, Portillo-Lemus et al. (2022) observed that self-pollen in the L-morph flowers stop growing lately (i.e., in the ovarian area) without fertilizing the ovules, concluding that a late-acting self-incompatible system (hereafter, LSI) is present in this morph.

At this point, it is relevant to understand the possible interactions between populations of different morphs in Lgh, and the implications that they may have on their expansive success in non-native areas in order to develop more effective management plans. To achieve this goal, Stoeckel et al. (2024) analyzed the population genetics in 53 Lgh populations in western Europe (without finding any Lpm population in the sampling area), 40 of which exclusively presented the L-morph and 13 the S-morph. This fact offered the opportunity to compare and interpret the differences between populations of different morphs in Lgh. Other previous works on genetic diversity of Lgh in peripatric or non-native areas pointed to a high clonality and an extremely low genetic diversity (Okada et al. 2009, Armitage et al. 2013), concluding in a monoclonal or few ancestral original clones for these invasive populations.

However, the investigations of Stoeckel et al. (2024) found a high genetic diversity in all populations of Lgh studied despite their predominant clonal reproduction. Interestingly, they found that sexual reproduction is also present, not only in the S-morph by selfing, but also in the L-morph, although limited and preferably by allogamy. They discuss the advantages and drawbacks of the different modes of reproduction observed in Lgh populations, the interactions among them, and the implications that both, the scarcely documented LSI (Gibbs 2014) and selfing, have in the reproductive success and in the maintenance of the high genetic diversity observed in Lgh in western Europe.

The contrasting results with the previous ones (Okada et al. 2009, Armitage et al. 2013) stress the relevance of using appropriate markers and analyses to assess the genetic diversity in autoployploid species, as well as the necessity of knowing the modes of reproduction in the populations studied for an optimal interpretation of the genetic metrics. The approach of the study by Stoeckel et al. (2024) had the challenge of having found suitable markers to deal with a taxon of complex origin such as Lgh, whose genome is compound by a set of autotetraploid chromosomes shared with Lpm and traces of ancient hybridizations of other diploid lineages (Barloy et al. 2024). Using RAD-Seq, Stoeckel et al. (2024) generated an original set of 36 polymorphic SNPs shared between Lgh and Lpm ensuring that these SNPs belong to the tetraploid part of the Lgh genome derived from Lpm. Another interesting contribution of this work is the exhaustive analysis of several genetic descriptors (indexes) and the interpretative guide they provide for each of them in relation to the different modes of reproduction of the study system. Finally, they propose a pair of very useful synthetic indices (i.e., clonality index and selfing index), since they allow to classify populations according to their levels of clonality and selfing.

Stoeckel et al. (2024) conclude the relevance that selfing and LSI populations, and the hybridization between them may have on the expansion and success of invasive plant species, and the necessity to know the modes of reproduction of these populations jointly with their genetic diversity in order to develop appropriate management plans. This study raises new questions such as the modes of reproduction and genetic diversity and structure have other Lgh populations, both invasive and native, and the dynamics of these populations under different future scenarios.

References

Armitage, J. D., Könyves, K., Bailey, J. P., David, J. C., & Culham, A. (2013). A molecular, morphological and cytological investigation of the identity of non-native Ludwigia (Onagraceae) populations in Britain. New Journal of Botany, 3(2), 88–95. https://doi.org/10.1179/2042349713Y.0000000023

Barloy, D., Lemus, L. P.-, Krueger-Hadfield, S. A., Huteau, V., & Coriton, O. (2024). Genomic relationships among diploid and polyploid species of the genus Ludwigia L. section Jussiaea using a combination of cytogenetic, morphological, and crossing investigations. ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2023.01.02.522458

Dandelot, S. (2004). Les Ludwigia spp. invasives du Sud de la France: Historique, Biosystématique, Biologie et Ecologie [PhD thesis, Aix-Marseille 3]. https://www.theses.fr/2004AIX30052

Dandelot, S., Verlaque, R., Dutartre, A., & Cazaubon, A. (2005). Ecological, dynamic and taxonomic problems due to Ludwigia (Onagraceae) in France. Hydrobiologia, 551(1), 131–136. https://doi.org/10.1007/s10750-005-4455-0

Gibbs, P. E. (2014). Late-acting self-incompatibility – the pariah breeding system in flowering plants. New Phytologist, 203(3), 717–734. https://doi.org/10.1111/nph.12874

Okada, M., Grewell, B. J., & Jasieniuk, M. (2009). Clonal spread of invasive Ludwigia hexapetala and L. grandiflora in freshwater wetlands of California. Aquatic Botany, 91(3), 123–129. https://doi.org/10.1016/j.aquabot.2009.03.006

Portillo Lemus, L. O., Bozec, M., Harang, M., Coudreuse, J., Haury, J., Stoeckel, S., & Barloy, D. (2021). Self-incompatibility limits sexual reproduction rather than environmental conditions in an invasive water primrose. Plant-Environment Interactions, 2(2), 74–86. https://doi.org/10.1002/pei3.10042

Portillo Lemus, L. O., Harang, M., Bozec, M., Haury, J., Stoeckel, S., & Barloy, D. (2022). Late-acting self-incompatible system, preferential allogamy and delayed selfing in the heteromorphic invasive populations of Ludwigia grandiflora subsp. hexapetala. Peer Community Journal, 2. https://doi.org/10.24072/pcjournal.108

Stoeckel, S., Becheler, R., Portillo-Lemus, L., Harang, M., Besnard, A.-L., Lassalle, G., Causse-Védrines, R., Michon-Coudouel, S., Park D. J., Pope, B. J., Petit, E. J. & Barloy, D. (2024) Reproductive modes in populations of late-acting self-incompatible and self-compatible polyploid Ludwigia grandiflora subsp. hexapetala in western Europe. biorxiv, ver.4 peer-reviewed and recommended by PCI Evol Biol https://doi.org/10.1101/2024.03.21.586104

It has long been known that most multicellular eukaryotes rely on microbial partners for a variety of functions including nutrition, immune reactions and defence against enemies. Lichens are probably the most popular example of a symbiosis involving a photosynthetic microorganism (an algae, a cyanobacteria or both) living embedded within the filaments of a fungus (usually an ascomycete). The latter is the backbone structure of the lichen, whereas the former provides photosynthetic products. Lichens are unique among symbioses because the structures the fungus and the photosynthetic microorganism form together do not resemble any of the two species living in isolation. Classic textbook examples like lichens are not often challenged and this is what Toby Spribille and his co-authors did with their paper published in July 2016 in Science [1]. This story started with the study of two species of macrolichens from the class of Lecanoromycetes that are commonly found in the mountains of Montana (US): Bryoria fremontii and B. tortuosa. For more than 90 years, these species have been known to differ in their chemical composition and colour, but studies performed so far failed in finding differences at the molecular level in both the mycobiont and the photobiont. These two species were therefore considered as nomenclatural synonyms, and the origin of their differences remained elusive. To solve this mystery, the authors of this work performed a transcriptome-wide analysis that, relative to previous studies, expanded the taxonomic range to all Fungi. This analysis revealed higher abundances of a previously unknown basidiomycete yeast from the genus Cyphobasidium in one of the lichen species, a pattern that was further confirmed by combining microscopy imaging and the fluorescent in situ hybridisation technique (FISH).

Finding out that a previously unknown micro-organism changes the colour and the chemical composition of an organism is surprising but not new. For instance, bacterial symbionts are able to trigger colour changes in some insect species [2], and endophyte fungi are responsible for the production of defensive compounds in the leaves of several grasses [3]. The study by Spribille and his co-authors is fascinating because it demonstrates that Cyphobasidium yeasts have played a key role in the evolution and diversification of Lecanoromycetes, one of the most diverse classes of macrolichens. Indeed these basidiomycete yeasts were not only found in Bryoria but in 52 other lichen genera from all six continents, and these included 42 out of 56 genera in the family Parmeliaceae. Most of these sequences formed a highly supported monophyletic group, and a molecular clock revealed that the origin of many macrolichen groups occurred around the same time Cyphobasidium yeasts split from Cystobasidium, their nearest relatives. This newly discovered passenger is therefore an ancient inhabitant of lichens and has driven the evolution of this emblematic group of organisms.

This study raises an important question on the stability of complex symbiotic partnerships. In intimate obligatory symbioses the evolutionary interests of both partners are often identical and what is good for one is also good for the other. This is the case of several insects that feed on poor diets like phloem and xylem sap, and which carry vertically-transmitted symbionts that provide essential nutrients. Molecular phylogenetic studies have repeatedly shown that in several insect groups transition to phloem or xylem feeding occurred at the same time these nutritional symbionts were acquired [4]. In lichens, an outstanding question is to know what was the key feature Cyphobasidium yeasts brought to the symbiosis. As suggested by the authors, these yeasts are likely to be involved in the production of secondary defensive metabolites and architectural structures, but, are these services enough to explain the diversity found in macrolichens? This paper is an appealing example of a multipartite symbiosis where the different partners share an ancient evolutionary history.

References

[1] Spribille T, Tuovinen V, Resl P, et al. 2016. Basidiomycete yeasts in the cortex of ascomycete macrolichens. Science 353:488–92. doi: 10.1126/science.aaf8287

[2] Tsuchida T, Koga R, Horikawa M, et al. 2010. Symbiotic Bacterium Modifies Aphid Body Color. Science 330:1102–1104. doi: 10.1126/science.1195463

[3] Clay K. 1988. Fungal Endophytes of Grasses: A Defensive Mutualism between Plants and Fungi. Ecology 69:10–16. doi: 10.2307/1943155

[4] Moran NA. 2007. Symbiosis as an adaptive process and source of phenotypic complexity. Proceeding of the National Academy of Science USA 104:8627–8633. doi: 10.1073/pnas.0611659104

In experimental evolution followed by whole genome resequencing, parallel evolution, defined as the increase in frequency of identical changes in independent populations adapting to the same environment, is often considered as the product of similar selection pressures and the parallel changes are interpreted as adaptive.
However, theory predicts that heterogeneity both in mutation rate and selection intensity across the genome can trigger patterns of parallel evolution. It is thus important to evaluate and quantify the contribution of both mutation and selection in determining parallel evolution to interpret more accurately experimental evolution genomic data and also potentially improve our capacity to predict the genes that will respond to selection.
In their manuscript, Bailey, Guo and Bataillon [1] derive a framework of statistical models to partition the role of mutation and selection in determining patterns of parallel evolution at the gene level. The rationale is to use the synonymous mutations dataset as a baseline to characterize the mutation rate heterogeneity, assuming a negligible impact of selection on synonymous mutations and then analyse the non-synonymous dataset to identify additional source(s) of heterogeneity, by examining the proportion of the variation explained by a number of genomic variables.
This framework is applied to a published data set of resequencing of 40 Saccharomyces cerevisiae populations adapting to a laboratory environment [2]. The model explaining at best the synonymous mutations dataset is one of homogeneous mutation rate along the genome with a significant positive effect of gene length, likely reflecting variation in the size of the mutational target. For the non-synonymous mutations dataset, introducing heterogeneity between sites for the probability of a change to increase in frequency is improving the model fit and this heterogeneity can be partially explained by differences in gene length, recombination rate and number of functional protein domains.
The application of the framework to an experimental data set illustrates its capacity to disentangle the role of mutation and selection and to identify genomic variables explaining heterogeneity in parallel evolution probability but also points to potential limits, cautiously discussed by the authors: first, the number of mutations in the dataset analysed needs to be sufficient, in particular to establish the baseline on the synonymous dataset. Here, despite a high replication (40 populations evolved in the exact same conditions), the total number of synonymous mutations that could be analysed was not very high and there was only one case of a gene with synonymous mutation in two independent populations. Second, although the models are able to identify factors affecting the mutation counts, the proportion of the variation explained is quite low. The consequence is that the models correctly predicts the mutation count distribution but the objective of predicting on which genes the response to selection will occur still seems quite far away.
The framework developed in this manuscript [1] clearly represents a very useful tool for the analysis of large “evolve and resequence” data sets and to gain a better understanding of the determinants of parallel evolution in general. The extension of its application to mutations others than SNPs would provide the possibility to get a more complete picture of the differences in contributions of mutation and selection intensity heterogeneities depending on the mutation types.

References

[1] Bailey SF, Guo Q and Bataillon T (2018) Identifying drivers of parallel evolution: A regression model approach. bioRxiv 118695, ver. 4 peer-reviewed by Peer Community In Evolutionary Biology. doi: 10.1101/118695

[2] Lang GI, Rice DP, Hickman, MJ, Sodergren E, Weinstock GM, Botstein D, and Desai MM (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature 500: 571–574. doi: 10.1038/nature12344