The advent of genome-wide association studies (GWAS) has been a great promise for our understanding of the connection between genotype and phenotype. Today, the NHGRI-EBI GWAS catalog contains 251,401 associations from 4,961 studies (1). This wealth of studies has also generated interest to use the summary statistics beyond the few top hits in order to make predictions for individuals without known phenotype, e.g. to predict polygenic risk scores or to study polygenic selection by comparing different groups. For instance, polygenic selection acting on the most studied polygenic trait, height, has been subject to multiple studies during the past decade (e.g. 2–6). They detected north-south gradients in Europe which were consistent with expectations. However, their GWAS summary statistics were based on the GIANT consortium data set, a meta-analysis of GWAS conducted in different European cohorts (7,8). The availability of large data sets with less stratification such as the UK Biobank (9) has led to a re-evaluation of those results. The nature of the GIANT consortium data set was realized to represent a potential problem for studies of polygenic adaptation which led several of the authors of the original articles to caution against the interpretations of polygenic selection on height (10,11). This was a great example on how the scientific community assessed their own earlier results in a critical way as more data became available. At the same time it left the question whether there is detectable polygenic selection separating populations more open than ever.

Generally, recent years have seen several articles critically assessing the portability of GWAS results and risk score predictions to other populations (12–14). Refoyo-Martínez et al. (15) are now presenting a systematic assessment on the robustness of cross-population signatures of polygenic adaptation in humans. They compiled GWAS results for complex traits which have been studied in more than one cohort and then use allele frequencies from the 1000 Genomes Project data (16) set to detect signals of polygenic score overdispersion. As the source for the allele frequencies is kept the same across all tests, differences between the signals must be caused by the underlying GWAS. The results are concerning as the level of overdispersion largely depends on the choice of GWAS cohort. Cohorts with homogenous ancestries show little to no overdispersion compared to cohorts of mixed ancestries such as meta-analyses. It appears that the meta-analyses fail to fully account for stratification in their data sets.

The authors based most of their analyses on the heavily studied trait height. Additionally, they use educational attainment (measured as the number of school years of an individual) as an example. This choice was due to the potential over- or misinterpretation of results by the media, the general public and by far right hate groups. Such traits are potentially confounded by unaccounted cultural and socio-economic factors. Showing that previous results about polygenic selection on educational attainment are not robust is an important result that needs to be communicated well. This forms a great example for everyone working in human genomics. We need to be aware that our results can sometimes be misinterpreted. And we need to make an effort to write our papers and communicate our results in a way that is honest about the limitations of our research and that prevents the misuse of our results by hate groups.

This article represents an important contribution to the field. It is cruicial to be aware of potential methodological biases and technical artifacts. Future studies of polygenic adaptation need to be cautious with their interpretations of polygenic score overdispersion. A recommendation would be to use GWAS results obtained in homogenous cohorts. But even if different biobank-scale cohorts of homogeneous ancestry are employed, there will always be some remaining risk of unaccounted stratification. These conclusions may seem sobering but they are part of the scientific process. We need additional controls and new, different methods than polygenic score overdispersion for assessing polygenic selection. Last year also saw the presentation of a novel approach using sequence data and GWAS summary statistics to detect directional selection on a polygenic trait (17). This new method appears to be robust to bias stemming from stratification in the GWAS cohort as well as other confounding factors. Such new developments show light at the end of the tunnel for the use of GWAS summary statistics in the study of polygenic adaptation.

References

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6. Racimo F, Berg JJ, Pickrell JK. Detecting polygenic adaptation in admixture graphs. Genetics. 2018. Arp;208(4):1565–1584. doi: https://doi.org/10.1534/genetics.117.300489

7. Lango Allen H, Estrada K, Lettre G, Berndt SI, Weedon MN, Rivadeneira F, et al. Hundreds of variants clustered in genomic loci and biological pathways affect human height. Nature. 2010 Oct;467(7317):832–8. doi: https://doi.org/10.1038/nature09410

8. Wood AR, Esko T, Yang J, Vedantam S, Pers TH, Gustafsson S, et al. Defining the role of common variation in the genomic and biological architecture of adult human height. Nat Genet. 2014 Nov;46(11):1173–86. doi: https://doi.org/10.1038/ng.3097

9. Bycroft C, Freeman C, Petkova D, Band G, Elliott LT, Sharp K, et al. The UK Biobank resource with deep phenotyping and genomic data. Nature. 2018 Oct;562(7726):203–9. doi: https://doi.org/10.1038/s41586-018-0579-z

10. Berg JJ, Harpak A, Sinnott-Armstrong N, Joergensen AM, Mostafavi H, Field Y, et al. Reduced signal for polygenic adaptation of height in UK Biobank. eLife. 2019 Mar 21;8:e39725. doi: https://doi.org/10.7554/eLife.39725

11. Sohail M, Maier RM, Ganna A, Bloemendal A, Martin AR, Turchin MC, et al. Polygenic adaptation on height is overestimated due to uncorrected stratification in genome-wide association studies. eLife. 2019 Mar 21;8:e39702. doi: https://doi.org/10.7554/eLife.39702

12. Martin AR, Kanai M, Kamatani Y, Okada Y, Neale BM, Daly MJ. Clinical use of current polygenic risk scores may exacerbate health disparities. Nature Genetics. 2019 Apr;51(4):584–91. doi: https://doi.org/10.1038/s41588-019-0379-x

13. Bitarello BD, Mathieson I. Polygenic Scores for Height in Admixed Populations. G3: Genes, Genomes, Genetics. 2020 Nov 1;10(11):4027–36. doi: https://doi.org/10.1534/g3.120.401658

14. Uricchio LH, Kitano HC, Gusev A, Zaitlen NA. An evolutionary compass for detecting signals of polygenic selection and mutational bias. Evolution Letters. 2019;3(1):69–79. doi: https://doi.org/10.1002/evl3.97

15. Refoyo-Martínez A, Liu S, Jørgensen AM, Jin X, Albrechtsen A, Martin AR, Racimo F. How robust are cross-population signatures of polygenic adaptation in humans? bioRxiv, 2021, 2020.07.13.200030, version 5 peer-reviewed and recommended by Peer community in Evolutionary Biology. doi: https://doi.org/10.1101/2020.07.13.200030

16. Auton A, Abecasis GR, Altshuler DM, Durbin RM, Abecasis GR, Bentley DR, et al. A global reference for human genetic variation. Nature. 2015 Sep 30;526(7571):68–74. doi: https://doi.org/10.1038/nature15393

17. Stern AJ, Speidel L, Zaitlen NA, Nielsen R. Disentangling selection on genetically correlated polygenic traits using whole-genome genealogies. bioRxiv. 2020 May 8;2020.05.07.083402. doi: https://doi.org/10.1101/2020.05.07.083402

The social amoeba Dictyostelium discoideum is an important model system for the study of cooperation and multicellularity as is has both unicellular and aggregative life phases. In the aggregative phase, which typically occurs when nutrients are limiting, individual cells eventually gather together to form a fruiting bodies whose spores may be dispersed to another, better, location and whose stalk cells, which support the spores, die. This extreme form of cooperation has been the focus of numerous studies that have revealed the importance genetic relatedness and kin selection (Hamilton 1964; Lehmann and Rousset 2014) in explaining the maintenance of this cooperative collective behavior (Strassmann et al. 2000; Kuzdzal-Fick et al. 2011; Strassmann and Queller 2011). However, much remains unknown with respect to how the interactions between individual cells, their neighbors, and their environment produce cooperative behavior at the scale of whole groups or collectives. In this preprint, Forget et al. (2021) describe how the D. discoideum system is crucial in this respect because it allows these cellular-level interactions to be studied in a systematic and tractable manner.
Spore bias, which is the tendency of a particular genotype or strain to disproportionately migrate to the spore instead of the stalk, is often used to define which strains are "cheaters" (positive spore bias) and which are "cooperative" (negative spore bias). Forget et al. (2021) note that spore bias depends on a number of stochastic factors including external drivers such as variation in environmental (or nutrient) quality and internal drivers like cell-cycle phase at the time of starvation. Spore bias is also affected by the social environment where the fraction of cheater strains in a spore may be limited by the ability of the remaining stalk cells to support the spore. The social environment can also affect cells through their differential responsiveness to the chemical factors that induce differentiation into stalk cells; responsiveness is partly a function of nutrient quality (Thompson and Kay 2000), which in turn can be a function of cell density. Thus, Forget et al. (2021) highlight a number of mechanisms that could generate frequency-dependent selection that would lead to the stable maintenance of multiple strains with different spore biases; in other words, both cheater and cooperative strains might stably coexist due to these cellular-level interactions.
The cellular-level interactions that Forget et al. (2021) highlight are particularly important because they pose a challenge evolutionary theory: some evolutionary models of social and collective behavior neglect or simplify these interactions. For example, Forget et al. (2021) note that the developmental, behavior, and environmental timescales relevant for Dictyostelium fruiting body formation all overlap. Evolutionary analyses often assume some of these timescales, for example developmental and behavior, are separate in order to simplify the analysis of any interactions. Thus, new theoretical work that allows these timescales to overlap may shed light on how cellular-level interactions can produce environmental, physiological, and behavioral feedbacks that drive the evolution of cooperation and other collective behaviors.

References

Forget, M., Adiba, S. and De Monte, S.(2021) Social conflicts in *Dictyostelium discoideum *: a matter of scales. HAL, hal-03088868, ver. 2 peer-reviewed and recommended by PCI Evolutionary Biology. https://hal.archives-ouvertes.fr/hal-03088868/

Hamilton, W. D. (1964). The genetical evolution of social behaviour. II. Journal of theoretical biology, 7(1), 17-52. doi: https://doi.org/10.1016/0022-5193(64)90039-6

Kuzdzal-Fick, J. J., Fox, S. A., Strassmann, J. E., and Queller, D. C. (2011). High relatedness is necessary and sufficient to maintain multicellularity in Dictyostelium. Science, 334(6062), 1548-1551. doi: https://doi.org/10.1126/science.1213272

Lehmann, L., and Rousset, F. (2014). The genetical theory of social behaviour. Philosophical Transactions of the Royal Society B: Biological Sciences, 369(1642), 20130357. doi: https://doi.org/10.1098/rstb.2013.0357

Strassmann, J. E., and Queller, D. C. (2011). Evolution of cooperation and control of cheating in a social microbe. Proceedings of the National Academy of Sciences, 108(Supplement 2), 10855-10862. doi: https://doi.org/10.1073/pnas.1102451108

Strassmann, J. E., Zhu, Y., & Queller, D. C. (2000). Altruism and social cheating in the social amoeba Dictyostelium discoideum. Nature, 408(6815), 965-967. doi: https://doi.org/10.1038/35050087

Thompson, C. R., & Kay, R. R. (2000). Cell-fate choice in Dictyostelium: intrinsic biases modulate sensitivity to DIF signaling. Developmental biology, 227(1), 56-64. doi: https://doi.org/10.1006/dbio.2000.9877

The role of microbial symbionts in governing social traits of their hosts is an exciting and developing research area. Just like symbionts influence host reproductive behaviour and can cause mating incompatibilities to promote symbiont transmission through host populations (Engelstadter and Hurst 2009; Correa and Ballard 2016; Johnson and Foster 2018) (see also discussion on conflict resolution in Johnsen and Foster 2018), microbial symbionts could enhance transmission by promoting the social behaviour of their hosts (Ezenwa et al. 2012; Lewin-Epstein et al. 2017; Gurevich et al. 2020). Here I apply the term ‘symbiosis’ in the broad sense, following De Bary 1879 as “the living together of two differently named organisms“ independent of effects on the organisms involved (De Bary 1879), i.e. the biological interaction between the host and its symbionts may include mutualism, parasitism and commensalism.
So far, we have relative few studies that explore the role of symbionts in promoting social behaviours such as parental care. Clearly, disentangling cause and effect when assessing the functional significance of symbiotic relationships in general is extremely challenging, and perhaps even more caution is needed when assessing the role of symbionts in the evolution of parental care, given the high fitness benefits to the offspring of receiving care. An interesting study on the symbiotic relationship between termites and their eukaryotic gut symbionts proposes a role of gut flagellates in the origin of subsocial behaviour (extended offspring care) in the termites through proctodeal trophallaxis (i.e. anus-to-mouth feeding), driven by mutualistic beneficial interactions (Nalepa 2020). Van Meyel et al. (2021) hypothesized a role of gut symbionts in promoting maternal care behaviour in the European earwig, and set out to test this idea in a carefully executed experimental study. They used a broad-spectrum antibiotic treatment to alter gut microbiota in mothers and examined its effect on maternal care provisioning. While the antibiotic treatment altered the gut microbiome, no effect on pre- or post-hatching maternal care was detected. The authors also investigated a broad range of physiological and reproductive traits measured over a major part of a female’s lifetime, and detected no effect of microbiome alteration on these traits. The study therefore does not provide evidence for a direct role of the gut microbiome in shaping offspring care in this population of European earwigs.
Within populations, earwigs show inter-individual variation in the expression of maternal care (Meunier et al. 2012; Ratz et al. 2016), and there is evidence that genetic and environmental factors contribute to this this variation (Meunier and Kolliker 2012; Kramer et al. 2017). The study by Van Meyel et al. (2021) is the first to analyse microbiome composition of the European earwig, and they study host-symbiont associations in a single population. A next step could be to explore among population variation in the gut microbiome, to achieve a better understanding on host-microbiome variation and dynamics in wild populations. Depending on the nature of host-symbiont associations across populations, new perspectives on their functional significance may arise (Hird 2017; Johnson and Foster 2018). It is therefore too early to conclusively confirm or reject the role of microbial symbionts in the expression of parental care in this system.

References

Correa, C. C., and Ballard, J. W. O. (2016). Wolbachia associations with insects: winning or losing against a master manipulator. Frontiers in Ecology and Evolution, 3, 153. doi: https://doi.org/10.3389/fevo.2015.00153

De Bary, A. (1879). Die Erscheinung der Symbiose. Verlag von Karl J. Trubner, Strassburg.

Engelstädter, J., and Hurst, G. D. (2009). The ecology and evolution of microbes that manipulate host reproduction. Annual Review of Ecology, Evolution, and Systematics, 40, 127-149. doi: https://doi.org/10.1146/annurev.ecolsys.110308.120206

Ezenwa, V. O., Gerardo, N. M., Inouye, D. W., Medina, M., and Xavier, J. B. (2012). Animal behavior and the microbiome. Science, 338(6104), 198-199. doi: https://doi.org/10.1126/science.1227412

Gurevich, Y., Lewin-Epstein, O., and Hadany, L. (2020). The evolution of paternal care: a role for microbes?. Philosophical Transactions of the Royal Society B, 375(1808), 20190599. doi: https://doi.org/10.1098/rstb.2019.0599

Hird, S. M. (2017). Evolutionary biology needs wild microbiomes. Frontiers in microbiology, 8, 725. doi: https://doi.org/10.3389/fmicb.2017.00725

Johnson, K. V. A., and Foster, K. R. (2018). Why does the microbiome affect behaviour?. Nature reviews microbiology, 16(10), 647-655. doi: https://doi.org/10.1038/s41579-018-0014-3

Kramer et al. (2017). When earwig mothers do not care to share: parent–offspring competition and the evolution of family life. Functional Ecology, 31(11), 2098-2107. doi: https://doi.org/10.1111/1365-2435.12915

Lewin-Epstein, O., Aharonov, R., and Hadany, L. (2017). Microbes can help explain the evolution of host altruism. Nature communications, 8(1), 1-7. doi: https://doi.org/10.1038/ncomms14040

Meunier, J., and Kölliker, M. (2012). Parental antagonism and parent–offspring co-adaptation interact to shape family life. Proceedings of the Royal Society B: Biological Sciences, 279(1744), 3981-3988. doi: https://doi.org/10.1098/rspb.2012.1416

Meunier, J., Wong, J. W., Gómez, Y., Kuttler, S., Röllin, L., Stucki, D., and Kölliker, M. (2012). One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig. Evolutionary Ecology, 26(3), 669-682. doi: https://doi.org/10.1007/s10682-011-9510-x

Nalepa, C. A. (2020). Origin of mutualism between termites and flagellated gut protists: transition from horizontal to vertical transmission. Frontiers in Ecology and Evolution, 8, 14. doi: https://doi.org/10.3389/fevo.2020.00014

Ratz, T., Kramer, J., Veuille, M., and Meunier, J. (2016). The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care. Oecologia, 182(2), 443-452. doi: https://doi.org/10.1007/s00442-016-3685-3

Van Meyel, S., Devers, S., Dupont, S., Dedeine, F. and Meunier, J. (2021) Alteration of gut microbiota with a broad-spectrum antibiotic does not impair maternal care in the European earwig. bioRxiv, 2020.10.08.331363. ver. 5 peer-reviewed and recommended by PCI Evol Biol. https://doi.org/10.1101/2020.10.08.331363

Historically neglected or considered a rare aberration in animals under the biological species concept, interspecific hybridisation has by now been recognised to be taxonomically widespread, particularly in rapidly diversifying groups (Dagilis et al. 2021; Edelman & Mallet 2021; Mallet et al. 2016; Seehausen 2004). Yet the prevalence of introgressive hybridizations, its evolutionary significance, and its impact on species diversification remain a hot topic of research in evolutionary biology. The rapid increase in genomic resources now available for non-model species has significantly contributed to the detection of introgressive hybridization across taxa showing that reticulated evolution is far more common in the animal kingdom than historically considered. Yet, detecting it, quantifying its magnitude, and assessing its evolutionary significance remains a challenging endeavour with constantly evolving methodologies to better explore and exploit genomic data (Blair & Ané 2020; Degnan & Rosenberg 2009; Edelman & Mallet 2021; Hibbins & Hahn 2022).

In the marine realm, the dearth of geographic barriers and the large dispersal abilities of pelagic species like cetaceans have raised the questions of how populations and species can diverge and adapt to distinct ecological conditions in face of potentially large gene-flow, the so-called marine speciation paradox (Bierne et al. 2003). Contemporaneous hybridization among cetacean species has been widely documented in nature despite large phenotypic differences (Crossman et al. 2016). The historical prevalence of reticulated evolution, its evolutionary significance, and how it might have impacted the evolutionary history and diversification of the cetaceans have however remained elusive so far. Recent phylogenomic studies suggested that introgression has been prevalent in cetacean evolutionary history with instances reported among baleen whales (mysticetes) (Árnason et al. 2018) and among toothed whales (odontocetes), especially in the rapidly diversifying dolphins family of the Delphininae (Guo et al. 2021; Moura et al. 2020).

Analysing publicly available whole-genome data from nine cetacean species across three families of Delphinoidae – dolphins, porpoises, and monondontidae – using phylogenomics and demo-genetics approaches, Westbury and colleagues (2022) take a step further in documenting that evolution among these species has been far from a simple bifurcating tree. Instead, their study describes widespread occurrences of introgression among Delphinoidae, drawing a complex picture of reticulated evolutionary history. After describing major topology discordance in phylogenetic gene trees along the genome, the authors use a panel of approaches to disentangle introgression from incomplete lineage sorting (ILS), the two most common causes of tree topology discordances (Hibbins & Hahn 2022). Applying popular tests that separate introgression from ILS, such as the Patterson’s D (a.k.a. ABBA-BABA) test (Durand et al. 2011; Green et al. 2010), QuIBL (Edelman et al. 2019), and D-FOIL (Pease & Hahn 2015), the authors report that signals of introgression are present in the genomes of most (if not all) the cetacean species included in their study. However, this picture needs to be nuanced. Most introgression signals seem to echo old introgression events that occurred primarily among ancestors. This is suggested by the differential signals of topology discordance along the genome when considering sliding windows along the genome of varying sizes (50kb, 100kb, and 1Mb), and by patterns of excess derived allele sharing along branches of the species tree, as captured by the f-branch test (Malinsky et al. 2021; Malinsky et al. 2018). The authors further investigated the dynamic of cessation of gene flow (and/or ILS) between species using the F1 hybrid PSMC (or hPSMC) approach (Cahill et al. 2016). By estimating the cross-coalescent rates (CRR) between species pairs with time in light of previously estimated species divergence times (McGowen et al. 2020), the authors report that gene flow (and/or ILS) most likely has stopped by now among most species, but it may have lasted for more than half of the time since the species split from each other. According to the author, this result may reflect the slow process by which reproductive isolation would have evolved between cetacean lineages, and that species isolation was marked by significant introgression events.

Now, while the present study provides a good overview of how complex is the reticulated evolutionary history of the Delphinoidae, getting a complete picture will require overcoming a few important limitations. The first ones are methodological and related to the phylogenomic analyses. Given the sampling design with one diploid genome per species, the authors could not phase the data into the parental haplotypes, but instead relied on a majority consensus creating mosaic haploidized genomes representing a mixture between the two parental copies. Moreover, by using large genomic windows (≥50kb) that likely span multiple independent loci, phylogenetic analyses in windows encompassed distinct phylogenetic signals, potentially leading to bias and inaccuracy in the inferences. Thawornwattana et al (2018) previously showed that this “concatenation approach”  could significantly impact phylogenetic inferences. They proposed instead to use loci small enough to minimise the risk of intra-locus recombination and to consider them in blocks of non-recombining loci along the genome in order to conduct phylogenetic analysed, ideally under the multi-species coalescent (MSC) that can account for ILS (e.g. BPP; Flouri et al. 2018; Jiao et al. 2020; Yang 2015). Such an approach applied to the diversification of the Delphinidae may reveal substantial changes compared to the currently admitted species tree.

Inaccuracy in the species tree estimation may have a major impact on the introgression analyses conducted in this study since the species tree and branching order must be supplied in the introgression analyses to properly disentangle introgression from ILS. Here, the authors rely on the tree topology that was previously estimated in McGowen et al. (2020), which they also recovered using their consensus estimation from ASTRAL-III (Zhang et al. 2018). While the methodologies accounted to a certain extent for ILS, albeit with potential bias induced by the concatenation approach, they ignore the presumably large amount of introgression among species during the diversification process. Estimating species branching order while ignoring introgression can lead to major bias in the phylogenetic inference and can lead to incorrect topologies. Even if these MSC-based methods account for ILS, inferences can become very inaccurate or even break down as gene flow increases (see for ex. Jiao et al. 2020; Müller et al. in press; Solís-Lemus et al. 2016). Dedicated approaches have been developed to model explicitly introgression together with ILS to estimate phylogenetic networks (Blair & Ané 2020; Rabier et al. 2021) or in isolation-with-migration model (Müller et al. in press; Wang et al. 2020). Future studies revisiting the reticulated evolutionary history of the Delphinoidae with such approaches may not only precise the species branching order, but also deliver a finer view of the magnitude and prevalence of introgression during the evolutionary history of these species.

A final part of Westbury et al. (2022)'s study set out to test whether historical periods of low abundance could have facilitated hybridization among Delphinoidae species. During these periods of low abundance, species may encounter only a limited number of conspecifics and may consider individuals from other species as suitable mating partners, leading to hybridisation (Crossman et al. 2016; Edwards et al. 2011; Westbury et al. 2019). The authors tested this hypothesis by considering genome-wide genetic diversity (or heterozygosity) as a proxy of historical effective population size (Ne), itself as a proxy of the evolution of census size with time. They also try to link historical Ne variation (from PSMC, Li & Durbin 2011) with their estimated time to cessation of gene flow or ILS (from the CRR of hPSMC). However, no straightforward relationship was found between the genetic diversity and the propensity of species to hybridize, nor was there any clear link between Ne variation through time and the cessation of gene flow or ILS. Such a lack of relationship may not come as a surprise, since the determinants of genome-wide genetic diversity and its variation through evolutionary time-scale are far more diverse and complex than just a direct link with hybridization, introgression, or even with the census population size. In fact, genetic diversity results from the balance between all the evolutionary processes at play in the species' evolutionary history (see the review of Ellegren & Galtier 2016). Other important factors can strongly impact genetic diversity, including demography and structure, but also linked selection (Boitard et al. 2022; Buffalo 2021; Ellegren & Galtier 2016). 

All in all, Westbury and coll. (2022) present here an interesting study providing an additional step towards resolving and understanding the complex evolutionary history of the Delphinoidae, and shedding light on the importance of introgression during the diversification of these cetacean species. Prospective work improving upon the taxonomic sampling, with additional genomic data for each species, considered with dedicated approaches tailored at estimating species tree or network while accounting for ILS and introgression will be key for refining the picture depicted in this study. Down the road, altogether these studies will contribute to assessing the evolutionary significance of introgression on the diversification of Delphinoides, and more generally on the diversification of cetacean species, which still remain an open and exciting perspective. 

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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
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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–
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