CONDAMINE Fabien's profile
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CONDAMINE Fabien

  • UMR 5554 Institut des Sciences de l'Evolution (Université de Montpellier), CNRS, Montpellier, France
  • Macroevolution, Paleontology, Phylogenetics / Phylogenomics, Phylogeography & Biogeography, Systematics / Taxonomy
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Recommendations:  2

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Recommendations:  2

2019-12-09
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Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snails

Recommended by based on reviews by Christelle Fraïsse, Pavel Matos and Niklas Wahlberg

The challenge of delineating species when they are hidden

The science of naming species (taxonomy) has been renewed with the developments of molecular sequencing, digitization of museum specimens, and novel analytical tools. However, naming species can be highly subjective, sometimes considered as an art [1], because it is based on human-based criteria that vary among taxonomists. Nonetheless, taxonomists often argue that species names are hypotheses, which are therefore testable and refutable as new evidence is provided. This challenge comes with a more and more recognized and critical need for rigorously delineated species not only for producing accurate species inventories, but more importantly many questions in evolutionary biology (e.g. speciation), ecology (e.g. ecosystem structure and functioning), conservation biology (e.g. targeting priorities) or biogeography (e.g. diversification processes) depend in part on those species inventories and our knowledge of species [2-3]. Inaccurate species boundaries or diversity estimates may lead us to deliver biased answers to those questions, exactly as phylogenetic trees must be reconstructed rigorously and analyzed critically because they are a first step toward discussing broader questions [2-3]. In this context, biological diversity needs to be studied from multiple and complementary perspectives requiring the collaboration of morphologists, molecular biologists, biogeographers, and modelers [4-5]. Integrative taxonomy has been proposed as a solution to tackle the challenge of delimiting species [2], especially in highly diverse and undocumented groups of organisms.
In an elegant study that harbors all the characteristics of an integrative approach, Alda et al. [6] tackle the delimitation of species within the snail genus Galba (Lymnaeidae). Snails of this genus represent a peculiar case study for species delineation with a long and convoluted taxonomic history in which previous works recognized a number of species ranging from 4 to 30. The confusion is likely due to a loose morphology (labile shell features and high plasticity), which makes the identification and naming of species very unstable and likely subjective. An integrative taxonomic approach was needed. After two decades of taxon sampling and visits of type localities, the authors present an impressively dense taxon sampling at a global scale for the genus, which includes all described species. When it comes to delineate species, taxon sampling is often the key if we want to embrace the genetic and morphological diversity. Molecular data was obtained for several types of markers (microsatellites and DNA sequences for four genes), which were combined to morphology of shell and of internal organs, and to geographic distribution. All the data are thoroughly analyzed with cutting-edge methods starting from Bayesian phylogenetic reconstructions using multispecies coalescent models, followed by models of species delimitation based on the molecular specimen-level phylogeny, and then Bayesian divergence time estimates. They also used probabilistic models of ancestral state estimation to infer the ancestral phenotypic state of the Galba ancestors.
Their numerous phylogenetic and delimitation analyses allow to redefine the species boundaries that indicate that the genus Galba comprises six species. Interestingly, four of these species are morphologically cryptic and likely constitute species with extensive genetic diversity and widespread geographic distribution. The other two species have more geographically restricted distributions and exhibit an alternative morphology that is more phylogenetically derived than the cryptic one. Although further genomic studies would be required to strengthen some species status, this novel delimitation of Galba species has important implications for our understanding of convergence and morphological stasis, or the role for stabilizing selection in amphibious habitats; topics that are rarely addressed with invertebrate groups. For instance, in terms of macroevolutionary history, it is striking that an invertebrate clade of that age (22 million years ago) has only given birth to six species today. Including 30 (ancient taxonomy) or 6 (integrative taxonomy) species in a similar amount of evolutionary time does not tell us the same story when studying the diversification processes [7]. Here, Alda et al. [6] present a convincing case study that should foster similar studies following their approach, which will provide stimulating perspectives for testing the concepts of species and their effects on evolutionary biology.

References

[1] Ohl, M. (2018). The art of naming. MIT Press.
[2] Dayrat, B. (2005). Towards integrative taxonomy. Biological Journal of the Linnean Society, 85(3), 407–415. doi: 10.1111/j.1095-8312.2005.00503.x
[3] De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56(6), 879–886. doi: 10.1080/10635150701701083
[4] Padial, J. M., Miralles, A., De la Riva, I., and Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7(1), 16. doi: 10.1186/1742-9994-7-16
[5] Schlick-Steiner, B. C., Steiner, F. M., Seifert, B., Stauffer, C., Christian, E., and Crozier, R. H. (2010). Integrative taxonomy: A multisource approach to exploring biodiversity. Annual Review of Entomology, 55(1), 421–438. doi: 10.1146/annurev-ento-112408-085432
[6] Alda, P. et al. (2019). Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snails. BioRxiv, 647867, v3 peer-reviewed and recommended by PCI Evolutionary Biology. doi: 10.1101/647867
[7] Ruane, S., Bryson, R. W., Pyron, R. A., and Burbrink, F. T. (2014). Coalescent species delimitation in milksnakes (Genus Lampropeltis) and impacts on phylogenetic comparative analyses. Systematic Biology, 63(2), 231–250. doi: 10.1093/sysbio/syt099

2018-06-05
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Pleistocene climate change and the formation of regional species pools

Recommended by based on reviews by 3 anonymous reviewers

Recent assembly of European biogeographic species pool

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

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CONDAMINE Fabien

  • UMR 5554 Institut des Sciences de l'Evolution (Université de Montpellier), CNRS, Montpellier, France
  • Macroevolution, Paleontology, Phylogenetics / Phylogenomics, Phylogeography & Biogeography, Systematics / Taxonomy
  • recommender

Recommendations:  2

Reviews:  0