Assessing population connectivity is central to understanding population dynamics, and is therefore of great importance in evolutionary biology and conservation biology. In the marine realm, the apparent absence of physical barriers, large population sizes and high dispersal capacities of most organisms often result in no detectable structure, thereby hindering inferences of population connectivity. In a review paper, Gagnaire et al. [1] propose several ideas to improve detection of population connectivity. Notably, using simulations they show that under certain circumstances introgression from one species into another may reveal cryptic population structure within that second species.
The isolated Kerguelen archipelago in the south of Indian Ocean represents a typical situation where the structure of coastal marine organisms is expected to be difficult to detect. In an elegant genomic study, Fraïsse et al. [2] take advantage of introgression from foreign lineages to infer fine-grained population structure in a population of mussels around the Kerguelen archipelago, and investigate its association with environmental variables. Using a large panel of genome-wide markers (GBS) and applying a range of methods that unravel patterns of divergence and gene flow among lineages, they first find that the Kerguelen population is highly admixed, with a major genetic background corresponding to the southern mussel lineage Mytilus platensis introgressed by three northern lineages. By selecting a panel of loci enriched in ancestry-informative SNPs (ie, SNPs highly differentiated among northern lineages) they then detect a fine-scale genetic structure around the Kerguelen archipelago, and identify a major connectivity break. They further show an associating between the genetic structure and environmental variables, particularly the presence of Macrocystis kelp, a marker of habitat exposure to waves (a feature repeatedly evidenced to be important for mussels). While such association pattern could lead to the interpretation that differentiated SNPs correspond to loci directly under selection or linked with such loci, and even be considered as support for adaptive introgression, Fraïsse et al. [2] convincingly show by performing simulations that the genetic-environment association detected can be entirely explained by dispersal barriers associated with environmental variables (habitat-associated connectivity). They also explain why the association is better detected by ancestry-informative SNPs as predicted by Gagnaire et al. [1]. In addition, intrinsic genetic incompatibilities, which reduce gene flow, tend to become trapped at ecotones due to ecological selection, even when loci causing genetic incompatibilities are unlinked with loci involved in adaption to local ecological conditions (Bierne et al. [3]’s coupling hypothesis), leading to correlations between environmental variables and loci not involved in local adaptation. Notably, in Fraïsse et al. [2]’s study, the association between the kelp and ancestry-informative alleles is not consistent throughout the archipelago, casting further doubt on the implication of these alleles in local adaptation.
The study of Fraïsse et al. [2] is therefore an important contribution to evolutionary biology because 1) it provides an empirical demonstration that alleles of foreign origin can be pivotal to detect fine-scale connectivity patterns and 2) it represents a test case of Bierne et al. [3]’s coupling hypothesis, whereby introgressed alleles also enhance patterns of genetic-environment associations. Since genomic scan or GWAS approaches fail to clearly reveal loci involved in local adaptation, how can we disentangle environment-driven selection from intrinsic reproductive barriers and habitat-associated connectivity? A related question is whether we can reliably identify cases of adaptive introgression, which have increasingly been put forward as a mechanism involved in adaptation [4]. Unfortunately, there is no easy answer, and the safest way to go is to rely – where possible – on independent information [5], in particular functional studies of the detected loci, as is for example the case in the mimetic butterfly Heliconius literature (e. g., [6]) where several loci controlling colour pattern variation are well characterized.

References

[1] Gagnaire, P.-A., Broquet, T., Aurelle, D., Viard, F., Souissi, A., Bonhomme, F., Arnaud-Haond, S., & Bierne, N. (2015). Using neutral, selected, and hitchhiker loci to assess connectivity of marine populations in the genomic era. Evolutionary Applications, 8, 769–786. doi: 10.1111/eva.12288
[2] Fraïsse, C., Haguenauer, A., Gerard, K., Weber, A. A.-T., Bierne, N., & Chenuil, A. (2018). Fine-grained habitat-associated genetic connectivity in an admixed population of mussels in the small isolated Kerguelen Islands. bioRxiv, 239244, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/239244
[3] Bierne, N., Welch, J., Loire, E., Bonhomme, F., & David, P. (2011). The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044–2072. doi: 10.1111/j.1365-294X.2011.05080.x
[4] Hedrick, P. W. (2013). Adaptive introgression in animals: examples and comparison to new mutation and standing variation as sources of adaptive variation. Molecular Ecology, 22, 4606–4618. doi: 10.1111/mec.12415
[5] Ravinet, M., Faria, R., Butlin, R. K., Galindo, J., Bierne, N., Rafajlović, M., Noor, M. A. F., Mehlig, B., & Westram, A. M. (2017). Interpreting the genomic landscape of speciation: a road map for finding barriers to gene flow. Journal of Evolutionary Biology, 30, 1450–1477. doi: 10.1111/jeb.13047.
[6] Jay, P., Whibley, A., Frézal, L., Rodríguez de Cara, M. A., Nowell, R. W., Mallet, J., Dasmahapatra, K. K., & Joron, M. (2018). Supergene evolution triggered by the introgression of a chromosomal inversion. Current Biology, 28, 1839–1845.e3. doi: 10.1016/j.cub.2018.04.072

Occasional events of asexual reproduction in otherwise sexual taxa have been documented since a long time. Accounts range from observations of offspring development from unfertilized eggs in Drosophila to rare offspring production by isolated females in lizards and birds (e.g., Stalker 1954, Watts et al 2006, Ryder et al. 2021). Many more such cases likely await documentation, as rare events are inherently difficult to observe. These rare events of asexual reproduction are often associated with low offspring fitness (“tychoparthenogenesis”), and have mostly been discarded in the evolutionary literature as reproductive accidents without evolutionary significance. Recently, however, there has been an increased interest in the details of evolutionary transitions from sexual to asexual reproduction (e.g., Archetti 2010, Neiman et al.2014, Lenormand et al. 2016), because these details may be key to understanding why successful transitions are rare, why they occur more frequently in some groups than in others, and why certain genetic mechanisms of ploidy maintenance or ploidy restoration are more often observed than others. In this context, the hypothesis has been formulated that regular or even obligate asexual reproduction may evolve from these rare events of asexual reproduction (e.g., Schwander et al. 2010).

A new study by Capdevielle Dulac et al. (2022) now investigates this question in a parasitoid wasp, highlighting also the fact that what is considered rare or occasional may differ from one system to the next. The results show “rare” parthenogenetic production of diploid daughters occurring at variable frequencies (from zero to 2 %) in different laboratory strains, as well as in a natural population. They also demonstrate parthenogenetic production of female offspring in both virgin females and mated ones, as well as no reduced fecundity of parthenogenetically produced offspring. These findings suggest that parthenogenetic production of daughters, while still being rare, may be a more regular and less deleterious reproductive feature in this species than in other cases of occasional asexuality. Indeed, haplodiploid organisms, such as this parasitoid wasp have been hypothesized to facilitate evolutionary transitions to asexuality (Neimann et al. 2014, Van Der Kooi et al. 2017). First, in haploidiploid organisms, females are diploid and develop from normal, fertilized eggs, but males are haploid as they develop parthenogenetically from unfertilized eggs. This means that, in these species, fertilization is not necessarily needed to trigger development, thus removing one of the constraints for transitions to obligate asexuality (Engelstädter 2008, Vorburger 2014). Second, spermatogenesis in males occurs by a modified meiosis that skips the first meiotic division (e.g., Ferree et al. 2019). Haploidiploid organisms may thus have a potential route for an evolutionary transition to obligate parthenogenesis that is not available to organisms: The pathways for the modified meiosis may be re-used for oogenesis, which might result in unreduced, diploid eggs. Third, the particular species studied here regularly undergoes inbreeding by brother-sister mating within their hosts. Homozygosity, including at the sex determination locus (Engelstädter 2008), is therefore expected to have less negative effects in this species compared to many other, non-inbreeding haplodipoids (see also Little et al. 2017). This particular species may therefore be less affected by loss of heterozygosity, which occurs in a fashion similar to self-fertilization under many forms of non-clonal parthenogenesis. 

Indeed, the study also addresses the mechanisms underlying parthenogenesis in the species. Surprisingly, the authors find that parthenogenetically produced females are likely produced by two distinct genetic mechanisms. The first results in clonality (maintenance of the maternal genotype), whereas the second one results in a loss of heterozygosity towards the telomeres, likely due to crossovers occurring between the centromeres and the telomeres. Moreover, bacterial infections appear to affect the propensity of parthenogenesis but are unlikely the primary cause. Together, the finding suggests that parthenogenesis is a variable trait in the species, both in terms of frequency and mechanisms. It is not entirely clear to what degree this variation is heritable, but if it is, then these results constitute evidence for low-frequency existence of variable and heritable parthenogenesis phenotypes, that is, the raw material from which evolutionary transitions to more regular forms of parthenogenesis may occur.

References

Archetti M (2010) Complementation, Genetic Conflict, and the Evolution of Sex and Recombination. Journal of Heredity, 101, S21–S33. https://doi.org/10.1093/jhered/esq009

Capdevielle Dulac C, Benoist R, Paquet S, Calatayud P-A, Obonyo J, Kaiser L, Mougel F (2022) Spontaneous parthenogenesis in the parasitoid wasp Cotesia typhae: low frequency anomaly or evolving process? bioRxiv, 2021.12.13.472356, ver. 6 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.12.13.472356

Engelstädter J (2008) Constraints on the evolution of asexual reproduction. BioEssays, 30, 1138–1150. https://doi.org/10.1002/bies.20833

Ferree PM, Aldrich JC, Jing XA, Norwood CT, Van Schaick MR, Cheema MS, Ausió J, Gowen BE (2019) Spermatogenesis in haploid males of the jewel wasp Nasonia vitripennis. Scientific Reports, 9, 12194. https://doi.org/10.1038/s41598-019-48332-9

van der Kooi CJ, Matthey-Doret C, Schwander T (2017) Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods. Evolution Letters, 1, 304–316. https://doi.org/10.1002/evl3.30

Lenormand T, Engelstädter J, Johnston SE, Wijnker E, Haag CR (2016) Evolutionary mysteries in meiosis. Philosophical Transactions of the Royal Society B: Biological Sciences, 371, 20160001. https://doi.org/10.1098/rstb.2016.0001

Little CJ, Chapuis M-P, Blondin L, Chapuis E, Jourdan-Pineau H (2017) Exploring the relationship between tychoparthenogenesis and inbreeding depression in the Desert Locust, Schistocerca gregaria. Ecology and Evolution, 7, 6003–6011. https://doi.org/10.1002/ece3.3103

Neiman M, Sharbel TF, Schwander T (2014) Genetic causes of transitions from sexual reproduction to asexuality in plants and animals. Journal of Evolutionary Biology, 27, 1346–1359. https://doi.org/10.1111/jeb.12357

Ryder OA, Thomas S, Judson JM, Romanov MN, Dandekar S, Papp JC, Sidak-Loftis LC, Walker K, Stalis IH, Mace M, Steiner CC, Chemnick LG (2021) Facultative Parthenogenesis in California Condors. Journal of Heredity, 112, 569–574. https://doi.org/10.1093/jhered/esab052

Schwander T, Vuilleumier S, Dubman J, Crespi BJ (2010) Positive feedback in the transition from sexual reproduction to parthenogenesis. Proceedings of the Royal Society B: Biological Sciences, 277, 1435–1442. https://doi.org/10.1098/rspb.2009.2113

Stalker HD (1954) Parthenogenesis in Drosophila. Genetics, 39, 4–34. https://doi.org/10.1093/genetics/39.1.4

Vorburger C (2014) Thelytoky and Sex Determination in the Hymenoptera: Mutual Constraints. Sexual Development, 8, 50–58. https://doi.org/10.1159/000356508

Watts PC, Buley KR, Sanderson S, Boardman W, Ciofi C, Gibson R (2006) Parthenogenesis in Komodo dragons. Nature, 444, 1021–1022. https://doi.org/10.1038/4441021a

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

Viruses establish intimate relationships with the cells they infect. The virocell is a novel entity, different from the original host cell and beyond the mere combination of viral and cellular genetic material. In these close encounters, viral and cellular genomes often hybridise, combine, recombine, merge and excise. Such chemical promiscuity leaves genomics scars that can be passed on to descent, in the form of deletions or duplications and, importantly, insertions and back and forth exchange of genetic material between viruses and their hosts.
In this preprint [1], Di Giovanni and coworkers report the identification of 13 genes present in the extant genomes of members of the Leptopilina wasp genus, bearing sound signatures of having been horizontally acquired from an ancestral virus. Importantly the authors identify Leptopilina boulardi filamentous virus (LbFV) as an extant relative of the ancestral virus that served as donor for the thirteen horizontally transferred genes. While pinpointing genes with a likely possible viral origin in eukaryotic genomes is only relatively rare, identifying an extant viral lineage related to the ancestral virus that continues to infect an extant relative of the ancestral host is remarkable. But the amazing evolutionary history of the Leptopilina hosts and these filamentous viruses goes beyond this shared genes. These wasps are endoparasitoids of Drosophila larvae, the female wasp laying the eggs inside the larvae and simultaneously injecting venom that hinders the immune response. The composition of the venoms is complex, varies between wasp species and also between individuals within a species, but a central component of all these venoms are spiked structures that vary in morphology, symmetry and size, often referred to as virus-like particles (VLPs).
In this preprint, the authors convincingly show that the expression pattern in the Leptopilina wasps of the thirteen genes identified to have been horizontally acquired from the LbFV ancestor coincides with that of the production of VLPs in the female wasp venom gland. Based on this spatio-temporal match, the authors propose that these VLPs have a viral origin. The data presented in this preprint will undoubtedly stimulate further research on the composition, function, origin, evolution and diversity of these VLP structures, which are highly debated (see for instance [2] and [3]).

References

[1] Di Giovanni, D., Lepetit, D., Boulesteix, M., Ravallec, M., & Varaldi, J. (2018). A behavior-manipulating virus relative as a source of adaptive genes for parasitoid wasps. bioRxiv, 342758, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/342758
[2] Poirié, M., Colinet, D., & Gatti, J. L. (2014). Insights into function and evolution of parasitoid wasp venoms. Current Opinion in Insect Science, 6, 52-60. doi: 10.1016/j.cois.2014.10.004
[3] Heavner, M. E., Ramroop, J., Gueguen, G., Ramrattan, G., Dolios, G., Scarpati, M., ... & Govind, S. (2017). Novel organelles with elements of bacterial and eukaryotic secretion systems weaponize parasites of Drosophila. Current Biology, 27(18), 2869-2877. doi: 10.1016/j.cub.2017.08.019

The evolution of selfing results from a balance between multiple evolutionary forces. Selfing provides an "automatic advantage" due to the higher efficiency of selfers to transmit their genes via selfed and outcrossed offspring. Selfed offspring, however, may suffer from inbreeding depression. In principle the ultimate evolutionary outcome is easy to predict from the relative magnitude of these two evolutionary forces [1,2]. Yet, several studies explicitly taking into account the genetic architecture of inbreeding depression noted that these predictions are often too restrictive because selfing can evolve in a broader range of conditions [3,4].
The present work by Abu Awad and Roze [5] provides an analytic understanding of these results. Abu Awad and Roze analyse the evolution of selfing in a multilocus model where some loci are coding for selfing while others are under direct selection. The evolution of selfing depends on (i) the classical benefit of selfing (automatic advantage), (ii) the cost of selfing due to inbreeding depression, (iii) the association between the loci coding for selfing and the loci under direct selection (likely to be positive because selfing is expected to be found in better purged genetic backgrounds) and (iv) the association between the loci coding for selfing and the linkage between loci under selection (this final term depends on the magnitude and the type of epistasis). Because these last two terms depend on genetic associations they are expected to play in when selection is strong and recombination is small. These last two terms explain why selfing is evolving under a range of conditions which is broader than predicted by earlier theoretical models. The match between the approximations for the different terms acting on the evolution of selfing and individual based simulations (for different fitness landscapes) is very convincing. In particular, this analysis also yields new results on the effect of different types of epistasis on inbreeding depression.
Another remarkable and important feature of this work is its readability. The analysis of multilocus models rely on several steps and approximations that often result in overwhelmingly complex papers. Abu Awad and Roze’s paper [5] is dense but it provides a very clear and comprehensive presentation of the interplay between multiple evolutionary forces acting on the evolution of selfing.

References

[1] Holsinger, K. E., Feldman, M. W., and Christiansen, F. B. (1984). The evolution of self-fertilization in plants: a population genetic model. The American Naturalist, 124(3), 446-453. doi: 10.1086/284287
[2] Lande, R., and Schemske, D. W. (1985). The evolution of self‐fertilization and inbreeding depression in plants. I. Genetic models. Evolution, 39(1), 24-40. doi: 10.1111/j.1558-5646.1985.tb04077.x
[3] Charlesworth, D., Morgan, M. T., and Charlesworth, B. (1990). Inbreeding depression, genetic load, and the evolution of outcrossing rates in a multilocus system with no linkage. Evolution, 44(6), 1469-1489. doi: 10.1111/j.1558-5646.1990.tb03839.x
[4] Uyenoyama, M. K., and Waller, D. M. (1991). Coevolution of self-fertilization and inbreeding depression I. Mutation-selection balance at one and two loci. Theoretical population biology, 40(1), 14-46. doi: 10.1016/0040-5809(91)90045-H
[5] Abu Awad, D. and Roze, D. (2020). Epistasis, inbreeding depression and the evolution of self-fertilization. bioRxiv, 809814, ver. 4 peer-reviewed and recommended by PCI Evol Biol. doi: 10.1101/809814