Genetic diversity is a key aspect of biodiversity and has important implications for evolutionary potential and thereby the persistence of species. Improving our understanding of the factors that drive genetic structure within and between populations is, therefore, a long-standing goal in evolutionary biology. However, this is a major challenge, because of the complex interplay between genetic drift, migration, and extinction/colonization dynamics on the one hand, and the biology and ecology of species on the other hand (Romiguier et al. 2014, Ellegren and Galtier 2016, Charlesworth 2003). 

Jarne et al. (2021) studied whether environmental and demographic factors affect the population genetic structure of four species of hermaphroditic freshwater snails in a similar way, using comparative analyses of neutral genetic microsatellite markers. 

Specifically, they investigated microsatellite variability of Hygrophila in almost 280 sites in Guadeloupe, Lesser Antilles, as part of a long-term survey experiment (Lamy et al. 2013). They then modelled the influence of the mating system, local environmental characteristics and demographic factors on population genetic diversity.

Consistent with theoretical predictions (Charlesworth 2003), they detected higher genetic variation in two outcrossing species than in two selfing species, emphasizing the importance of the mating system in maintaining genetic diversity. The study further identified an important role of site connectivity, through its influences on effective population size and extinction/colonisation events. Finally, the study detects an influence of interspecific interactions caused by an ongoing invasion by one of the studied species on genetic structure, highlighting the indirect effect of changes in community composition and demography on population genetics.

Jarne et al. (2021) could address the extent to which genetic structure is determined by demographic and environmental factors in multiple species given the remarkable sampling available. Additionally, the study system is extremely suitable to address this hypothesis as species’ habitats are defined and delineated. Whilst the authors did attempt to test for across-species correlations, further investigations on this matter are required. Moreover, the effect of interactions between factors should be appropriately considered in any modelling between genetic structure and local environmental or demographic features.

The findings in this study contribute to improving our understanding of factors influencing population genetic diversity, and highlights the complexity of interacting factors, therefore also emphasizing the challenges of drawing general implications, additionally hampered by the relatively limited number of species studied. Jarne et al. (2021) provide an excellent showcase of an empirical framework to test determinants of genetic structure in natural populations. As such, this study can be an example for further attempts of comparative analysis of genetic diversity.

References

Charlesworth, D. (2003) Effects of inbreeding on the genetic diversity of populations. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 358, 1051-1070. doi: https://doi.org/10.1098/rstb.2003.1296

Ellegren, H. and Galtier, N. (2016) Determinants of genetic diversity. Nature Reviews Genetics, 17, 422-433. doi: https://doi.org/10.1038/nrg.2016.58

Jarne, P., Lozano del Campo, A., Lamy, T., Chapuis, E., Dubart, M., Segard, A., Canard, E., Pointier, J.-P. and David, P. (2021) Connectivity and selfing drives population genetic structure in a patchy landscape: a comparative approach of four co-occurring freshwater snail species. HAL, hal-03295242, ver. 2 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://hal.archives-ouvertes.fr/hal-03295242

Lamy, T., Gimenez, O., Pointier, J. P., Jarne, P. and David, P. (2013). Metapopulation dynamics of species with cryptic life stages. The American Naturalist, 181, 479-491. doi: https://doi.org/10.1086/669676

Romiguier, J., Gayral, P., Ballenghien, M. et al. (2014) Comparative population genomics in animals uncovers the determinants of genetic diversity. Nature, 515, 261-263. doi: https://doi.org/10.1038/nature13685

Jean Cury and colleagues (2021) have developed a protocol to simulate bacterial evolution in SLiM. In contrast to existing methods that depend on the coalescent, SLiM simulates evolution forward in time. SLiM has, up to now, mostly been used to simulate the evolution of eukaryotes (Haller and Messer 2019), but has been adapted here to simulate evolution in bacteria. Forward-in-time simulations are usually computationally very costly. To circumvent this issue, bacterial population sizes are scaled down. One would now expect results to become inaccurate, however, Cury et al. show that scaled-down forwards simulations provide very accurate results (similar to those provided by coalescent simulators) that are consistent with theoretical expectations. Simulations were analyzed and compared to existing methods in simple and slightly more complex scenarios where recombination affects evolution. In all scenarios, simulation results from coalescent methods (fastSimBac (De Maio and Wilson 2017), ms (Hudson 2002)) and scaled-down forwards simulations were very similar, which is very good news indeed.

A biologist not aware of the complexities of forwards, backwards simulations and the coalescent, might now naïvely ask why another simulation method is needed if existing methods perform just as well. To address this question the manuscript closes with a very neat example of what exactly is possible with forwards simulations that cannot be achieved using existing methods. The situation modeled is the growth and evolution of a set of 50 bacteria that are randomly distributed on a petri dish. One side of the petri dish is covered in an antibiotic the other is antibiotic-free. Over time, the bacteria grow and acquire antibiotic resistance mutations until the entire artificial petri dish is covered with a bacterial lawn. This simulation demonstrates that it is possible to simulate extremely complex (e.g. real world) scenarios to, for example, assess whether certain phenomena are expected with our current understanding of bacterial evolution, or whether there are additional forces that need to be taken into account. Hence, forwards simulators could significantly help us to understand what current models can and cannot explain in evolutionary biology.  

References  

Cury J, Haller BC, Achaz G, Jay F (2021) Simulation of bacterial populations with SLiM. bioRxiv, 2020.09.28.316869, version 5 peer-reviewed and recommended by Peer community in Evolutionary Biology.  https://doi.org/10.1101/2020.09.28.316869

De Maio N, Wilson DJ (2017) The Bacterial Sequential Markov Coalescent. Genetics, 206, 333–343. https://doi.org/10.1534/genetics.116.198796

Haller BC, Messer PW (2019) SLiM 3: Forward Genetic Simulations Beyond the Wright–Fisher Model. Molecular Biology and Evolution, 36, 632–637. https://doi.org/10.1093/molbev/msy228

Hudson RR (2002) Generating samples under a Wright–Fisher neutral model of genetic variation. Bioinformatics, 18, 337–338. https://doi.org/10.1093/bioinformatics/18.2.337

One can only hope that one day, we will be able to evaluate how the ecological complexity surrounding natural populations affects their ability to adapt. This is more like a long term quest than a simple scientific aim. Many steps are heading in the right direction. This paper by Monroe and colleagues (2021) is one of them.
Many ecological and genetic mechanisms shape the evolutionary potential of phenotypic trait variation and many of them involve environmental heterogeneity (Pujol et al 2018). To date, we cannot look into these ecological and genetic mechanisms without oversimplifying their effects. We often look into trait variation one trait at a time albeit the variation of multiple phenotypic traits is often linked at the genetic or environmental level. As a consequence, we put our conclusions at risk by not accounting for the reciprocal impacts of trait changes upon each other (Teplitsky et al 2014). We also usually restrict the study of a continuous gradient of environmental conditions to a few conditions because it would otherwise be impossible to model its environmental effect. As a consequence, we miss the full picture of the continuous often nonlinear phenotypic plastic response. Whether the trait undergo threshold effect changes thereby remains obscured to us. Collectively, these issues impede our ability to understand how selection shapes the ecological strategy of organisms under variable environments.
In this paper, Monroe and colleagues (2021) propose an original approach that raised to these two challenges. They analysed phenotypic plastic changes in response to a continuous environment in a multidimensional trait space, namely the response of Brachypodium plant developmental and physiological traits to a continuous gradient of soil moisture. They used dry down experimental treatments to produce the continuous soil moisture gradient and compared the plant capacity to use water between annual B. distachyon and perennial B. sylvaticum. Their results revealed the best mathematical functions that model the nonlinear curvature of the continuous plastic response of Brachypodium plants. This work reinforces our view that nonlinear plastic responses can result in greater or lesser trait values at any stage of the environmental gradient that were unexpected on the basis of linear predictors (Gienapp and Brommer 2014). Their findings also imply that different threshold responses characterize different genotypes. These could otherwise have been missed by a classical approach. By shedding light on unforeseen interactions between traits that make their correlation vary along the nonlinear response, they were able to describe more accurately Brachypodium ecological strategies and the changes in evolutionary constraints along the soil moisture gradient.
Their empirical approach allows to test what environmental conditions maximises the opportunity for selection to shape trait variation. For example, it revealed unforeseen divergence in potentially adaptive mechanisms or life history strategies – and not just trait values – between annual and perennial species of Brachypodium. Behind every environmental variation of the constraints to the future evolutionary change of multiple traits, we can expect that the evolutionary history of the populations shaped their trait genetic correlations. Investigating the nonlinear signature of adaptive evolution across continuous environments will get us into uncharted territory.
Our ability to predict the adaptive potential of species is limited. With their approach of continuous environmental gradients beyond linearity, Monroe and collaborators (2021) improve our understanding of plant phenotypic responses and open a brand new range of exciting developments. As they mention: "the opportunity for scaling up" their approach is big. To illustrate this prospect, I can easily think of an example: the quantitative genetic random regression model. This model allows to use any degree of genetic relatedness in a wild population to estimate the genetic variation of phenotypic plastic reaction norms (Nussey et al 2007, Pujol and Galaud 2013). However, in this approach, only a few modalities of the environmental gradient are used to model nonlinear phenotypic plastic responses. From there, it is rather intuitive. Combining the best of these two approaches (continuity of genetic relatedness in the wild & continuity of environmental gradient in experiments) could open ground breaking new perspectives in research.

References

Gienapp P. & J.E. Brommer. 2014. Evolutionary dynamics in response to climate change. In: Charmentier A, Garant D, Kruuk LEB, editors. Quantitative genetics in the wild. Oxford: Oxford University Press, Oxford. pp. 254–273. doi: https://doi.org/10.1093/acprof:oso/9780199674237.003.0015
Monroe, J. G., Cai, H., and Des Marais, D. L. (2020). Trait plasticity and covariance along a continuous soil moisture gradient. bioRxiv, 2020.02.17.952853, ver. 5 peer-reviewed and recommended by PCI Evol Biol. doi: https://doi.org/10.1101/2020.02.17.952853
Pujol et al. (2018). The missing response to selection in the wild. Trends in ecology & evolution, 33(5), 337-346. doi: https://doi.org/10.1016/j.tree.2018.02.007
Pujol, B., and Galaud, J. P. (2013). A practical guide to quantifying the effect of genes underlying adaptation in a mixed genomics and evolutionary ecology approach. Botany Letters, 160(3-4), 197-204. doi: https://doi.org/10.1080/12538078.2013.799045
Nussey, D. H., Wilson, A. J., and Brommer, J. E. (2007). The evolutionary ecology of individual phenotypic plasticity in wild populations. Journal of evolutionary biology, 20(3), 831-844. doi: https://doi.org/10.1111/j.1420-9101.2007.01300.x
Teplitsky et al. (2014). Assessing multivariate constraints to evolution across ten long-term avian studies. PLoS One, 9(3), e90444. doi: https://doi.org/10.1371/journal.pone.0090444

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

Nearly 8 million people are suffering from Chagas disease in the Americas. The etiological agent, Trypanosoma cruzi, is mainly transmitted by triatomine bugs, also known as kissing or vampire bugs, which suck blood and transmit the parasite through their feces. Among these triatomine species, Rhodnius prolixus is considered the main vector, and many studies have focused on characterizing its biology, physiology, ecology and evolution. 

Interestingly, given that Rhodnius species feed almost exclusively on blood, their diet is unbalanced, and the insects can lack nutrients and vitamins that they cannot synthetize themself, such as B-vitamins. In all insects feeding exclusively on blood, symbioses with microbes producing B-vitamins (mainly biotin, riboflavin and folate) have been widely described (see review in Duron and Gottlieb 2020) and are critical for insect development and reproduction. These co-evolved relationships between blood feeders and nutritional symbionts could now be considered to develop new control methods, by targeting the ‘Achille’s heel’ of the symbiotic association (i.e., transfer of nutrient and / or control of nutritional symbiont density). But for this, it is necessary to better characterize the relationships between triatomines and their symbionts. 

R. prolixus is known to be associated with several symbionts. The extracellular gut symbiont Rhodococcus rhodnii, which reaches high bacterial densities and is almost fixed in R. prolixus populations, appears to be a nutritional symbiont under many blood sources. This symbiont can provide B-vitamins such as biotin (B7), niacin (B3), thiamin (B1), pyridoxin (B6) or riboflavin (B2) and can play an important role in the development and the reproduction of R. prolixus (Pachebat et al. (2013) and see review in Salcedo-Porras et al. (2020)). This symbiont is orally acquired through egg smearing, ensuring the fidelity of transmission of the symbiont from mother to offspring. However, as recently highlighted by Tobias et al. (2020) and Gilliland et al. (2022), other gut microbes could also participate to the provision of B-vitamins, and R. rhodnii could additionally provide metabolites (other than B-vitamins) increasing bug fitness. In the study from Filée et al., the authors focused on Wolbachia, an intracellular, maternally inherited bacterium, known to be a nutritional symbiont in other blood-sucking insects such as bedbugs (Nikoh et al. 2014), and its potential role in vitamin provision in triatomine bugs. 

After screening 17 different triatomine species from the 3 phylogenetic groups prolixus, pallescens and pictipes, they first show that Wolbachia symbionts are widely distributed in the different Rhodnius species. Contrary to R. rhodnii that were detected in all samples, Wolbachia prevalence was patchy and rarely fixed. The authors then sequenced, assembled, and compared 13 Wolbachia genomes from the infected Rhodnius species. They showed that all Wolbachia are phylogenetically positioned in the supergroup F that contains wCle (the Wolbachia from bedbugs). In addition, 8 Wolbachia strains (out of 12) encode a biotin operon under strong purifying selection, suggesting the preservation of the biological function and the metabolic potential of Wolbachia to supplement biotin in their Rhodnius host. From the study of insect genomes, the authors also evidenced several horizontal transfers of genes from Wolbachia to Rhodnius genomes, which suggests a complex evolutionary interplay between vampire bugs and their intracellular symbiont. 

This nice piece of work thus provides valuable information to the fields of multiple partners / nutritional symbioses and Wolbachia research. Dual symbioses described in insects feeding on unbalanced diets generally highlight a certain complementarity between symbionts that ensure the whole nutritional complementation. The study presented by Filée et al. leads rather to consider the impact of multiple symbionts with different lifestyles and transmission modes in the provision of a specific nutritional benefit (here, biotin). Because of the low prevalence of Wolbachia in certain species, a “ménage à trois” scenario would rather be replaced by an “open couple”, where the host relationship with new symbiotic partners (more or less stable at the evolutionary timescale) could provide benefits in certain ecological situations. The results also support the potential for Wolbachia to evolve rapidly along a continuum between parasitism and mutualism, by acquiring operons encoding critical pathways of vitamin biosynthesis.

References

Duron O. and Gottlieb Y. (2020) Convergence of Nutritional Symbioses in Obligate Blood Feeders. Trends in Parasitology 36(10):816-825. https://doi.org/10.1016/j.pt.2020.07.007

Filée J., Agésilas-Lequeux K., Lacquehay L., Bérenger J.-M., Dupont L., Mendonça V., Aristeu da Rosa J. and Harry M. (2023) Wolbachia genomics reveals a potential for a nutrition-based symbiosis in blood-sucking Triatomine bugs. bioRxiv, 2022.09.06.506778, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2022.09.06.506778

Gilliland C.A. et al. (2022) Using axenic and gnotobiotic insects to examine the role of different microbes on the development and reproduction of the kissing bug Rhodnius prolixus (Hemiptera: Reduviidae). Molecular Ecology. https://doi.org/10.1111/mec.16800

Nikoh et al. (2014) Evolutionary origin of insect–Wolbachia nutritional mutualism. PNAS. 111(28):10257-10262. https://doi.org/10.1073/pnas.1409284111

Pachebat, J.A. et al. (2013). Draft genome sequence of Rhodococcus rhodnii strain LMG5362, a symbiont of Rhodnius prolixus (Hemiptera, Reduviidae, Triatominae), the principle vector of Trypanosoma cruzi. Genome Announc. 1(3):e00329-13. https://doi.org/10.1128/genomea.00329-13

Salcedo-Porras N., et al. (2020). The role of bacterial symbionts in Triatomines: an evolutionary perspective. Microorganisms. 8:1438. https://doi.org/10.3390%2Fmicroorganisms8091438

Tobias N.J., Eberhard F.E., Guarneri A.A. (2020) Enzymatic biosynthesis of B-complex vitamins is supplied by diverse microbiota in the Rhodnius prolixus anterior midgut following Trypanosoma cruzi infection. Computational and Structural Biotechnology Journal. 3395-3401. https://doi.org/10.1016/j.csbj.2020.10.031