Phylogeography is celebrating its 35th birthday; Geogenomics its 8th. We asked authors of papers in a recent special section of Journal of Biogeography to reflect on how these two approaches can increase our understanding of the distributions of genetic diversity.
Above: Cover for the Geogenomics virtual issue .
Biogeography is an integrative discipline, as is reflected in familiar conjunctions including bio⋅geography, phylo⋅geography, and macro⋅ecology. One recently introduced term — geo⋅genomics — represents interdisciplinary approaches using “large-scale genetic data to test or to constrain geological hypotheses” (sensu Baker et al. 2014, p.38). Geogenomics is eight years young, arguably in its foundational phase, and its relationship with other disciplines in biogeography is developing. A special section in the Journal of Biogeography — which is running for the three months (v.49.9–49.11) and being compiled into a virtual issue — reviews the origins of geogenomics and compiles a suite of new studies that reflect geogenomics’ current purview (as practiced by biogeographers). A major contention of this special section is that Geogenomics has potential to substantially change the way we combine genetics and geology to increase rigor and insight when answering biogeographic questions. Here, we provide perspectives from some of the authors of papers in the special section on what they see in the future for Geogenomics. We posed three questions to them:
– What are the predominant limitations on (or opportunities for) advances in Phylogeography?
– What do you find new and exciting about Geogenomics?
– Can Geogenomics change the future of Phylogeography? (And/or what else will be needed?)
Their answers, and links to their papers, are provided below. We hope the special section and this discussion provoke thought and stimulate advances in this rich area. We look forward to publishing more on these topics in the coming years!
Editorial: (Free to read online for a year.)
Dawson, M.N., Ribas, C.C., Dolby, G.A. and Fritz, S.C. (2022) Geogenomics: Toward synthesis. J Biogeogr. 49(9):1657–1661. https://doi.org/10.1111/jbi.14467
The special section on Geogenomics was conceived and edited by Paul Baker (Duke University, USA), Greer Dolby (University of Alabama at Birmingham, USA), Sherilyn Fritz (University of Nebraska – Lincoln, USA), Anna Papadopoulou (University of Cyprus, Cyprus), and Camila Ribas (Instituto Nacional de Pesquisas da Amazônia, Brazil) in association with the chief editors.
Key attributes in geogenomic thinking include the bidirectionality of process and inference, and the integrative iteration of ecological, evolutionary, and earth processes, scaling from generational to geological times. See Dawson et al. (2022) for more detail.
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Barbosa, W. E. S., Ferreira, M., Schultz, E. D., Luna, L. W., Laranjeiras, T. O., Aleixo, A., & Ribas, C. C. (2022). Habitat association constrains population history in two sympatric ovenbirds along Amazonian floodplains. Journal of Biogeography, 49, 1683– 1695. https://doi.org/10.1111/jbi.14266
Molecular biology has advanced a lot in the last decade, and the development of new sequencing techniques and a decrease in sequencing costs made a lot of phylogenomic studies possible. Given the availability of different sequencing platforms and sequencing strategies, strategic planning in phylogenomic studies has become more difficult, and analysis of all these data remains at a high cost. In addition, such complex data analysis requires scientists to be trained in bioinformatics, which makes them capable of solving the problems that arise throughout the stages of data processing and analysis.
What I find most exciting about geogenomics is the possibility of comparing dates of geological or climatic events with biological data at various scales with robust data, which allows even more accurate reconstructions of Earth‘s history.
Geogeonomics can make phylogeographic studies more interdisciplinary. In phylogeographic studies, biologists use dating and geological interpretations to understand the processes governing the distribution of closely related lineages. Meanwhile, in geogenomics, geologists can use genomic data as a proxy for their earth history studies. Thus, through bioinformatics, biologists and geologists can work together to test hypotheses as well as formulate new ones and obtain increasingly robust reconstructions.
– Waleska Barbosa
Northern chamois (Rupicapra rupicapra) inhabit steep terrain in Central Europe and are well-adapted to cold climate. They recolonized the European Alps after the glaciation. Photo credit: Flurin Leugger.
Leugger, F., Broquet, T., Karger, D. N., Rioux, D., Buzan, E., Corlatti, L., Crestanello, B., Curt-Grand-Gaudin, N., Hauffe, H. C., Rolečková, B., Šprem, N., Tissot, N., Tissot, S., Valterová, R., Yannic, G. & Pellissier, L.(2022). Dispersal and habitat dynamics shape the genetic structure of the Northern chamois in the Alps. Journal of Biogeography, 49, 1848– 1861. https://doi.org/10.1111/jbi.14363
Phylogeographic studies at the very beginning were purely descriptive, linking molecular data to geography, e.g., investigating the spatial distribution of genotypes (Avise et al., 1987[1]). Early phylogeographic studies were based on mtDNA markers which included only few 100s base pairs and only describe female-related patterns (Avise 1998[2], 2009[3]). Compared to the multi-locus or more recently used whole genome analyses (see also response below), they provide limited insights into the history of the study organism. Advances in statistical approaches and modelling helped to overcome some limitations, i.e., to receive more realistic estimations or investigate additional species-environment relations (Knowles, 2009[4]) and test hypothesis of genetic diversity over time. The spatio-temporal resolution of genetic and/or geographic data is until now often a limiting factor in phylogeographic studies.
The connection of genomic (i.e., data from entire genomes and not only from a very restricted marker) data and landscape evolution at large spatial scales is exciting in the field of Geogenomics. Although initially defined as way to investigate geological patterns based on biological data (Baker et al., 2014[1]), Geogenomics is often perceived in a reciprocal illumination: geological or geographic data is used to improve our understanding of biodiversity and biological properties (Dawson et al., 2022[2]). New insights can be obtained by combining genomic with geographic data (and various models) compared to classical genetic analysis. For example, we[3] used genomic data of chamois across the European Alps in combination with several hundred landscape connectivity models over 20,000 years to test hypothesis on chamois’ dispersal which would not have been possible with distribution data or genetic data alone. Given that many researches use the reciprocal definition of Geogenomics (e.g., Barbosa et al., 2021[4]; Luna et al., 2021[5]; Ortego et al., 2022[6]), I argue that Geogenomics should be considered as part – or rather advancement – and not opposite of Phylogeography, where whole-genome data is used compared to the single or few genetic markers used during the emergence of Phylogeography. The core of Geogenomics is to test various hypothesis using genomic data in combination with both models and landscape data to gain new insights into biodiversity (e.g., migration) and landscape evolution (e.g., formation of migration barriers). Understanding how biodiversity evolved facing past environmental changes is paramount to predict and/or mitigate adverse effects of the current global changes where Geogenomics can contribute valuable information.
The core of Geogenomics is the hypothesis-driven approach using large-scale genomic data to improve our understanding of geological or biological properties. Advancements in genetic analysis and computational modelling are likely to foster Geogenomics in the next years and result in ever more hypothesis which can be addressed. Additionally, the tools of Geogenomics offer new possibilities to study biodiversity and landscape evolution at a finer scale than ever before. Genomic (whole-genome) data, i.e., SNP-based approaches, allows for more detailed analysis compared to classical phylogeographic studies, that is for example, on population level instead and over shorter time to estimate anthropogenic impacts. Using ancient DNA (aDNA) from fossils will offer new insights into Phylogeography. For example, aDNA could improve models about historic population changes and connectivity between populations.
– Flurin Leugger
(Left) The Striped Woodcreeper (Xiphorhynchus obsoletus, Dendrocolaptidae), a bird species with wide distribution in the Amazon floodplains. Photo: João S. Barros. (Right) Amazonian floodplains of the Rio Branco, at the foot of the Serra Grande, Roraima, Brazil. Photo: Thiago O. Laranjeiras.
Luna, L. W., Ribas, C. C., & Aleixo, A. (2022). Genomic differentiation with gene flow in a widespread Amazonian floodplain-specialist bird species. Journal of Biogeography, 49, 1670– 1682. https://doi.org/10.1111/jbi.14257
Modern phylogeography still lacks conceptual and methodological definitions in incorporating multivariate data (e.g., environmental, biotic, behavioral, climatic, and geological variables) into biogeographic models. In this context, the predominant limitation is how we can incorporate information from multiple species traits and historical changes in the landscape (constrained by dated geological events) into a statistical framework that can infer the current distribution of genetic diversity of the species and communities. Another issue is that the incorporation of whole genomes into the discipline has just begun, and several new tools and approaches will have to be developed or adjusted to fully incorporate the massive amount of data provided by this type of DNA sequencing.
Geogenomics can be seen as a step forward in phylogeography in terms of concept and methodological approach. This advance comes from defining the study design more rigorously, using geological constraints and high-throughput genomic technology to tackle biogeographic hypotheses. That is, it adds the context of geological history into the investigation of biogeographic patterns, or vice versa, using known biogeographic patterns to illuminate geological processes at both regional and intercontinental scales.
Explicitly using dated geological events within phylogeographic approaches can help refine the hypotheses being tested. For the past two decades, phylogeography relied on the description of spatial genetic patterns as a posteriori explanation of possible events that shaped the evolutionary histories of taxa. With the addition of concepts from geogenomics, phylogeography can be profoundly changed, whereby the addition of an explicit historical/geological context into sampling designs will help illuminate complex evolutionary and biogeographic patterns.
– Leilton Luna & Alexandre Aleixo
The thermophilous grasshopper Dericorys carthagonovae. Photograph by Francisco Rodríguez.
Ortego, J., González-Serna, M. J., Noguerales, V., & Cordero, P. J. (2022). Genomic inferences in a thermophilous grasshopper provide insights into the biogeographic connections between northern African and southern European arid-dwelling faunas. Journal of Biogeography, 49, 1696– 1710. https://doi.org/10.1111/jbi.14267
In my opinion, an important limitation is the difficulty to integrate geological information into process-based phylogeographic inference, which is particularly challenging when ancient events are involved. Geology and phylogeography illuminate each other, but what is probably needed is more active collaboration between researchers of the two disciplines. Among others, this could help to consider more carefully uncertainty surrounding geological reconstructions when interpreting phylogeographic evidence (e.g., dating of events).
Something I find very exciting are the discrepancies between geology/geography and phylogenomic evidence, as such findings can provide important counterintuitive insights into disregarded phenomena governing species distributions and geographical diversification. For instance, mounting biogeographical evidence – including our study published in this special issue – suggests that the colonization of semiarid areas of Iberia by thermophilous organisms of African origin most likely took place from the central Maghreb region (Algeria or Tunisia). This indicates that the exchange of terrestrial organisms between Iberia and Africa did not exclusively take place across the strait of Gibraltar (i.e., through the shortest geographical distance) and suggests that long-distance overseas dispersal might be much more common than previously thought.
Understanding the processes shaping species distributions and their spatial patterns of genomic variation requires the effective integration of multiple disciplines and, as such, geogenomics will be instrumental to the advance of phylogeography. However, organismal traits (i.e., dispersal capacity, interspecific interactions, ecology, etc.) must be also considered to formulate and test phylogeographic hypotheses, as not all taxa are expected to respond in the same way to a shared abiotic background and only certain geological events (e.g., Quaternary climatic oscillations) but not others (e.g., landmass/ocean configuration) might explain their demographic and evolutionary trajectories depending on species-specific attributes. Phylogeographic studies on geophilic organisms with low dispersal capacity might particularly benefit from a “geogenomic approach” and provide insights that, in turn, could contribute to refine geological hypotheses, particularly when developed within a multi-species comparative framework.
– Joaquín Ortego
Additional information:
Virtual issue on Geogenomics: https://onlinelibrary.wiley.com/doi/toc/10.1111/(ISSN)1365-2699.Geogenomics
REFERENCES
[1] Baker, P. A., Fritz, S. C., Dick, C. W., Eckert, A. J., Horton, B. K., Manzoni, S., … & Battisti, D. S. (2014). The emerging field of geogenomics: constraining geological problems with genetic data. Earth-Science Reviews, 135, 38-47.
[2] Dawson, M.N., Ribas, C.C., Dolby, G.A. and Fritz, S.C. (2022), Geogenomics: Toward synthesis. Journal of Biogeography, 49, 1657-1661.
[3] Leugger, F., Broquet, T., Karger, D. N., Rioux, D., Buzan, E., Corlatti, L., … & Pellissier, L. (2022). Dispersal and habitat dynamics shape the genetic structure of the Northern chamois in the Alps. Journal of Biogeography 49, 1848– 1861. https://doi.org/10.1111/jbi.14363
[4] Elizangela dos Santos Barbosa, W., Ferreira, M., de Deus Schultz, E., Willians Luna, L., Orsi Laranjeiras, T., Aleixo, A., & Cherem Ribas, C. Habitat association constrains population history in two sympatric ovenbirds along Amazonian floodplains. Journal of Biogeography, 49, 1683-1695.
[5] Luna, L. W., Ribas, C. C., & Aleixo, A. (2021). Genomic differentiation with gene flow in a widespread Amazonian floodplain‐specialist bird species. Journal of Biogeography, 49, 1670-1682.
[6] Ortego, J., González‐Serna, M. J., Noguerales, V., & Cordero, P. J. (2022). Genomic inferences in a thermophilous grasshopper provide insights into the biogeographic connections between northern African and southern European arid‐dwelling faunas. Journal of Biogeography, 49, 1696-1710.