We currently live in the Anthropocene, the geological age characterized by a profound impact of human populations in the ecosystems and the environment. While there is little doubt about the action of humans in the shaping of present landscapes, it can be difficult to determine what the state of those landscapes was before humans started to modify them. This is the case of the Madagascar grasslands, whose origins have been debated with arguments proposing them either as anthropogenic, created with the arrival of humans around 2000BP, or as ancient features of the natural landscape with a forest fragmentation process due to environmental changes pre-dating human arrival [e.g. 1,2]. One way to clarify this question is through the genetic study of native species. Population continuity and fragmentation along time shape the structure of the genetic diversity in space. Species living in a uniform continuous habitat are expected to show genetic structuring determined only by geographical distance. Recent changes of the habitat can take many generations to reshape that genetic structure [3]. Thus, we expect genetic structure to reflect ancient features of the landscape.

The work by Jordi Salmona and collaborators [4] studies the factors determining the population genetic structure of the Malagasy spiny olive (Noronhia spinifolia). This narrow endemic species is distributed in the discontinuous forest patches of the Loky-Manambato region (northern Madagascar). Jordi Salmona and collaborators genotyped 72 individuals distributed across the species distribution with restriction associated DNA sequencing and organelle microsatellite markers. Then, they studied the population genetic structure of the species. Using isolation-by-resistance models [5], they tested the influence of several landscape features (forest cover, roads, rivers, slope, etc.) on the connectivity between populations. Maternally inherited loci (chloroplast and mitochondria) and bi-parentally inherited loci (nuclear), were analysed separately in an attempt to identify the role of pollen and seed dispersal in the connectivity of populations.

Despite the small distribution of the species, Jordi Salmona and collaborators [4] found remarkable levels of genetic diversity. The spatial structure of this diversity was found to be mainly explained by the forest cover of the landscape, suggesting that the landscape has been composed by patches of forests and grasslands for a long time. The main role of forest cover for the connectivity among populations also highlights the importance of riparian forest as dispersal corridors. Finally, differences between organelle and nuclear markers were not enough to establish any strong conclusion about the differences between pollen and seed dispersal.

The results presented by Jordi Salmona and collaborators [4] contribute to the understanding of the history and ecology of understudied Madagascar ecosystems. Previous population genetic studies  in some forest-dwelling mammals have been interpreted as supporting an old age for the fragmented landscapes in northern Madagascar [e.g. 1,6]. To my knowledge, this is the first study on a tree species. While this work might not completely settle the debate, it emphasizes the importance of studying a diversity of species to understand the biogeographic dynamics of a region.

References

1. Quéméré, E., X. Amelot, J. Pierson, B. Crouau-Roy, L. Chikhi (2012) Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the United States of
America 109: 13028–13033. https://doi.org/10.1073/pnas.1200153109
2. Joseph, G.S., C.L. Seymour (2020) Madagascan highlands: originally woodland and forest containing endemic grasses, not grazing-adapted grassland. Proceedings of the Royal Society B: Biological Sciences 287: 20201956. https://doi.org/10.1098/rspb.2020.1956
3. Landguth, E.L., S.A. Cushman, M.K. Schwartz, K.S. McKelvey, M. Murphy, G. Luikart (2010) Quantifying the lag time to detect barriers in landscape genetics. Molecular Ecology 19: 4179–
4191. https://doi.org/10.1111/j.1365-294X.2010.04808.x
4. Salmona J., Dresen A, Ranaivoson AE, Manzi S, Pors BL, Hong-Wa C, Razanatsoa J, Andriaholinirina NV, Rasoloharijaona S, Vavitsara M-E, Besnard G (2021) How ancient forest fragmentation and riparian connectivity generate high levels of genetic diversity in a micro-endemic Malagasy tree. bioRxiv, 2020.11.25.394544, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.11.25.394544
5. McRae, B.H. (2006) Isolation by resistance. Evolution 60: 1551–1561. https://doi.org/10.1111/j.0014-3820.2006.tb00500.x
6. Rakotoarisoa J.-E., M. Raheriarisena, S.M. Goodman (2013) Late Quaternary climatic vegetational shifts in an ecological transition zone of northern Madagascar: insights from genetic analyses of two endemic rodent species. Journal of Evolutionary Biology 26: 1019–1034. https://doi.org/10.1111/jeb.12116

Each individual multicellular organism, each of our bodies, is a small universe. Every living surface -skin, cuticle, bark, mucosa- is the home place to milliards of bacteria, fungi and viruses. They constitute our microbiota. Some of them are essential for certain organisms. Other could not live without their hosts. For many species, the relationship between host and microbiota is so close that their histories are inseparable. The recognition of this biological inextricability has led to the notion of holobiont as the organism ensemble of host and microbiota. When individuals of a particular animal or plant species expand their geographical range, it is the holobiont that expands. And these processes of migration, expansion and colonization are often accompanied by evolutionary and ecological innovations in the interspecies relationships, at the macroscopic level (e.g. novel predator-prey or host-parasite interactions) and at the microscopic level (e.g. changes in the microbiota composition). From the human point of view, these novel interactions can be economically disastrous if they involve and threaten important crop or cattle species. And this is especially worrying in the present context of genetic standardization and intensification for mass-production on the one hand, and of climate change on the other.

With this perspective, the international team led by Amandine Cornille presents a study aiming at understanding the evolutionary history of the rosy apple aphid Dysaphis plantaginea Passerini, a major pest of the cultivated apple tree Malus domestica Borkh (1). The apple tree was probably domesticated in Central Asia, and later disseminated by humans over the world in different waves, and it was probably introduced in Europe by the Greeks. It is however unclear when and where D. plantaginea started parasitizing the cultivated apple tree. The ancestral D. plantaginea could have already infected the wild ancestor of current cultivated apple trees, but the aphid is not common in Central Asia. Alternatively, it may have gained access only later to the plant, possibly via a host jump, from Pyrus to Malus that may have occurred in Asia Minor or in the Caucasus. In the present preprint, Olvera-Vázquez and coworkers have analysed over 650 D. plantaginea colonies from 52 orchards in 13 countries, in Western, Central and Eastern Europe as well as in Morocco and the USA. The authors have analysed the genetic diversity in the sampled aphids, and have characterized as well the composition of the associated endosymbiont bacteria. The analyses detect substantial recent admixture, but allow to identify aphid subpopulations slightly but significantly differentiated and isolated by distance, especially those in Morocco and the USA, as well as to determine the presence of significant gene flow. This process of colonization associated to gene flow is most likely indirectly driven by human interactions. Very interestingly, the data show that this genetic diversity in the aphids is not reflected by a corresponding diversity in the associated microbiota, largely dominated by a few Buchnera aphidicola variants. In order to determine polarity in the evolutionary history of the aphid-tree association, the authors have applied approximate Bayesian computing and machine learning approaches. Albeit promising, the results are not sufficiently robust to assess directionality nor to confidently assess the origin of the crop pest. Despite the large effort here communicated, the authors point to the lack of sufficient data (in terms of aphid isolates), especially originating from Central Asia. Such increased sampling will need to be implemented in the future in order to elucidate not only the origin and the demographic history of the interaction between the cultivated apple tree and the rosy apple aphid. This knowledge is needed to understand how this crop pest struggles with the different seasonal and geographical selection pressures while maintaining high genetic diversity, conspicuous gene flow, differentiated populations and low endosymbiontic diversity.

References

1. Olvera-Vazquez SG, Remoué C, Venon A, Rousselet A, Grandcolas O, Azrine M, Momont L, Galan M, Benoit L, David GM, Alhmedi A, Beliën T, Alins G, Franck P, Haddioui A, Jacobsen SK, Andreev R, Simon S, Sigsgaard L, Guibert E, Tournant L, Gazel F, Mody K, Khachtib Y, Roman A, Ursu TM, Zakharov IA, Belcram H, Harry M, Roth M, Simon JC, Oram S, Ricard JM, Agnello A, Beers EH, Engelman J, Balti I, Salhi-Hannachi A, Zhang H, Tu H, Mottet C, Barrès B, Degrave A, Razmjou J, Giraud T, Falque M, Dapena E, Miñarro M, Jardillier L, Deschamps P, Jousselin E, Cornille A (2021) Large-scale geographic survey provides insights into the colonization history of a major aphid pest on its cultivated apple host in Europe, North America and North Africa. bioRxiv, 2020.12.11.421644, ver. 3 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.12.11.421644

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

​​Durability of plant resistance to diploid pathogen Hirohisa Kishino Based on the population genetic and epidemiologic model, Saubin et al. (2021) report that the resistant hosts generated by the breeding based on the gene-for-gene interaction is durable much longer against diploid pathogens than haploid pathogens. The avr allele of pathogen that confers the resistance is genetically recessive. The heterozygotes are not recognized by the resistant hosts and only the avr/avr homozygote is adaptive. As a result, the trajectory of avr allele frequency becomes more stochastic due to genetic drift. Although the paper focuses on the evolution of standing polymorphism, it seems obvious that the adaptive mutations in pathogen have much larger probability of being deleted from the population because the individuals own the avr allele mostly in the form of heterozygote at the initial phase after the mutation. Since only few among many models of plant resistance deployment study the case of diploid pathogen and the contribution of the pathogen life cycle, this work will add an important intellect to the literature (Rimbaud et al. 2021).

From the study of host-parasite interaction in flax rust Melampsora lini, Flor (1942, 1955) showed that the host resistance is formed by the interaction of a host resistance gene and a corresponding pathogen gene. This gene-for-gene hypothesis has been supported by experimental evidence and has served as a basis of the methods of molecular breeding targeting the dominant R genes. However, modern agriculture provides the pathogen populations with the homogeneous environments and laid strong selection pressure on them. As a result, the newly developed resistant plants face the risk of immediate resistance breakdown (Möller and Stukenbrock 2017).

Currently, quantitative resistance is getting attention as characters as a potential target for long-life (mild) resistant breeds (Lannou, 2012). They are polygenic and controlled partly by the same genes that mediate qualitative resistance but mostly by the genes that encode defense-related outputs such as strengthening of the cell wall or defense compound biosynthesis (Corwin and Kliebenstein, 2017). Progress of molecular genetics may overcome the technical difficulty (Bakkeren and Szabo, 2020). Saubin et al. (2021) notes that the pattern of genetic inheritance of the pathogen counterparts that respond to the host traits is crucial regarding with the durability of the resistant hosts. The resistance traits for which avr alleles are predicted to be recessive may be the targets of breeding.

References

Bakkeren, G., and Szabo, L. J. (2020) Progress on molecular genetics and manipulation of rust fungi. Phytopathology, 110, 532-543. https://doi.org/10.1094/PHYTO-07-19-0228-IA

Corwin, J. A., and Kliebenstein, D. J. (2017) Quantitative resistance: more than just perception of a pathogen. The Plant Cell, 29, 655-665. https://doi.org/10.1105/tpc.16.00915

Flor, H. H. (1942) Inheritance of pathogenicity in a cross between physiological races 22 and 24 of Melampsova lini. Phytopathology, 35. Abstract.

Flor, H. H. (1955) Host-parasite interactions in flax rust-its genetics and other implications. Phytopathology, 45, 680-685.

Lannou, C. (2012) Variation and selection of quantitative traits in plant pathogens. Annual review of phytopathology, 50, 319-338. https://doi.org/10.1146/annurev-phyto-081211-173031

Möller, M. and Stukenbrock, E. H. (2017) Evolution and genome architecture in fungal plant pathogens. Nature Reviews Microbiology. 15, 756–771. https://doi.org/10.1038/nrmicro.2017.76

Rimbaud, L., Fabre, F., Papaïx, J., Moury, B., Lannou, C., Barrett, L. G., and Thrall, P. H. (2021) Models of Plant Resistance Deployment. Annual Review of Phytopathology, 59. https://doi.org/10.1146/annurev-phyto-020620-122134

Saubin, M., De Mita, S., Zhu, X., Sudret, B. and Halkett, F. (2021) Impact of ploidy and pathogen life cycle on resistance durability. bioRxiv, 2021.05.28.446112, ver. 4 peer-reviewed and recommended by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2021.05.28.446112

In recent years many studies have documented shifts in phenology in response to climate change, be it in arrival times in migrating birds, budset in trees, adult emergence in butterflies, or flowering time in annual plants (Coen et al. 2018; Piao et al. 2019). While these changes are, in part, explained by phenotypic plasticity, more and more studies find that they involve also genetic changes, that is, they involve evolutionary change (e.g., Metz et al. 2020). Yet, evolutionary change may occur through genetic drift as well as selection. Therefore, in order to demonstrate adaptive evolutionary change in response to climate change, drift has to be excluded as an alternative explanation (Hansen et al. 2012). A new study by Gay et al. (2021) shows just how difficult this can be. 

The authors investigated a recent evolutionary shift in flowering time by in a population an annual plant that reproduces predominantly by self-fertilization. The population has recently been subjected to increased temperatures and reduced rainfalls both of which are believed to select for earlier flowering times. They used a “resurrection” approach (Orsini et al. 2013; Weider et al. 2018): Genotypes from the past (resurrected from seeds) were compared alongside more recent genotypes (from more recently collected seeds) under identical conditions in the greenhouse. Using an experimental design that replicated genotypes, eliminated maternal effects, and controlled for microenvironmental variation, they found said genetic change in flowering times: Genotypes obtained from recently collected seeds flowered significantly (about 2 days) earlier than those obtained 22 generations before. However, neutral markers (microsatellites) also showed strong changes in allele frequencies across the 22 generations, suggesting that effective population size, Ne, was low (i.e., genetic drift was strong), which is typical for highly self-fertilizing populations. In addition, several multilocus genotypes were present at high frequencies and persisted over the 22 generations, almost as in clonal populations (e.g., Schaffner et al. 2019). The challenge was thus to evaluate whether the observed evolutionary change was the result of an adaptive response to selection or may be explained by drift alone. 

Here, Gay et al. (2021) took a particularly careful and thorough approach. First, they carried out a selection gradient analysis, finding that earlier-flowering plants produced more seeds than later-flowering plants. This suggests that, under greenhouse conditions, there was indeed selection for earlier flowering times. Second, investigating other populations from the same region (all populations are located on the Mediterranean island of Corsica, France), they found that a concurrent shift to earlier flowering times occurred also in these populations. Under the hypothesis that the populations can be regarded as independent replicates of the evolutionary process, the observation of concurrent shifts rules out genetic drift (under drift, the direction of change is expected to be random). 

The study may well have stopped here, concluding that there is good evidence for an adaptive response to selection for earlier flowering times in these self-fertilizing plants, at least under the hypothesis that selection gradients estimated in the greenhouse are relevant to field conditions. However, the authors went one step further. They used the change in the frequencies of the multilocus genotypes across the 22 generations as an estimate of realized fitness in the field and compared them to the phenotypic assays from the greenhouse. The results showed a tendency for high-fitness genotypes (positive frequency changes) to flower earlier and to produce more seeds than low-fitness genotypes. However, a simulation model showed that the observed correlations could be explained by drift alone, as long as Ne is lower than ca. 150 individuals. The findings were thus consistent with an adaptive evolutionary change in response to selection, but drift could only be excluded as the sole explanation if the effective population size was large enough. 

The study did provide two estimates of Ne (19 and 136 individuals, based on individual microsatellite loci or multilocus genotypes, respectively), but both are problematic. First, frequency changes over time may be influenced by the presence of a seed bank or by immigration from a genetically dissimilar population, which may lead to an underestimation of Ne (Wang and Whitlock 2003). Indeed, the low effective size inferred from the allele frequency changes at microsatellite loci appears to be inconsistent with levels of genetic diversity found in the population. Moreover, high self-fertilization reduces effective recombination and therefore leads to non-independence among loci. This lowers the precision of the Ne estimates (due to a higher sampling variance) and may also violate the assumption of neutrality due to the possibility of selection (e.g., due to inbreeding depression) at linked loci, which may be anywhere in the genome in case of high degrees of self-fertilization. 

There is thus no definite answer to the question of whether or not the observed changes in flowering time in this population were driven by selection. The study sets high standards for other, similar ones, in terms of thoroughness of the analyses and care in interpreting the findings. It also serves as a very instructive reminder to carefully check the assumptions when estimating neutral expectations, especially when working on species with complicated demographies or non-standard life cycles. Indeed the issues encountered here, in particular the difficulty of establishing neutral expectations in species with low effective recombination, may apply to many other species, including partially or fully asexual ones (Hartfield 2016). Furthermore, they may not be limited to estimating Ne but may also apply, for instance, to the establishment of neutral baselines for outlier analyses in genome scans (see e.g, Orsini et al. 2012). 

References

Cohen JM, Lajeunesse MJ, Rohr JR (2018) A global synthesis of animal phenological responses to climate change. Nature Climate Change, 8, 224–228. https://doi.org/10.1038/s41558-018-0067-3

Gay L, Dhinaut J, Jullien M, Vitalis R, Navascués M, Ranwez V, Ronfort J (2021) Evolution of flowering time in a selfing annual plant: Roles of adaptation and genetic drift. bioRxiv, 2020.08.21.261230, ver. 4 recommended and peer-reviewed by Peer Community in Evolutionary Biology. https://doi.org/10.1101/2020.08.21.261230

Hansen MM, Olivieri I, Waller DM, Nielsen EE (2012) Monitoring adaptive genetic responses to environmental change. Molecular Ecology, 21, 1311–1329. https://doi.org/10.1111/j.1365-294X.2011.05463.x

Hartfield M (2016) Evolutionary genetic consequences of facultative sex and outcrossing. Journal of Evolutionary Biology, 29, 5–22. https://doi.org/10.1111/jeb.12770

Metz J, Lampei C, Bäumler L, Bocherens H, Dittberner H, Henneberg L, Meaux J de, Tielbörger K (2020) Rapid adaptive evolution to drought in a subset of plant traits in a large-scale climate change experiment. Ecology Letters, 23, 1643–1653. https://doi.org/10.1111/ele.13596

Orsini L, Schwenk K, De Meester L, Colbourne JK, Pfrender ME, Weider LJ (2013) The evolutionary time machine: using dormant propagules to forecast how populations can adapt to changing environments. Trends in Ecology & Evolution, 28, 274–282. https://doi.org/10.1016/j.tree.2013.01.009

Orsini L, Spanier KI, Meester LD (2012) Genomic signature of natural and anthropogenic stress in wild populations of the waterflea Daphnia magna: validation in space, time and experimental evolution. Molecular Ecology, 21, 2160–2175. https://doi.org/10.1111/j.1365-294X.2011.05429.x

Piao S, Liu Q, Chen A, Janssens IA, Fu Y, Dai J, Liu L, Lian X, Shen M, Zhu X (2019) Plant phenology and global climate change: Current progresses and challenges. Global Change Biology, 25, 1922–1940. https://doi.org/10.1111/gcb.14619

Schaffner LR, Govaert L, De Meester L, Ellner SP, Fairchild E, Miner BE, Rudstam LG, Spaak P, Hairston NG (2019) Consumer-resource dynamics is an eco-evolutionary process in a natural plankton community. Nature Ecology & Evolution, 3, 1351–1358. https://doi.org/10.1038/s41559-019-0960-9

Wang J, Whitlock MC (2003) Estimating Effective Population Size and Migration Rates From Genetic Samples Over Space and Time. Genetics, 163, 429–446. PMID: 12586728

Weider LJ, Jeyasingh PD, Frisch D (2018) Evolutionary aspects of resurrection ecology: Progress, scope, and applications—An overview. Evolutionary Applications, 11, 3–10. https://doi.org/10.1111/eva.12563