Section: Evolutionary Biology
Topic: Evolution, Genetics/Genomics, Population biology
Phylogeographic breaks and how to find them: An empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal
10.24072/pcjournal.301 - Peer Community Journal, Volume 3 (2023), article no. e74.
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Aim: Discontinuity in the distribution of genetic diversity (often based on mtDNA) is usually interpreted as evidence for phylogeographic breaks, underlying vicariant units. However, a misleading signal of phylogeographic break can arise in the absence of barrier to gene flow, under mechanisms of isolation by distance (IBD). How and under which conditions phylogeographic breaks can be reliably differentiated from populations evolving under IBD remain unclear. Here, we use multi-locus sequence data from a widely distributed lizard species to address these questions in an empirical setting. Location: Morocco. Taxon: Spiny-footed lizard (Acanthodactylus erythrurus), Squamata: Lacertidae. Methods: Using 325 samples from 40 localities, we identified genetic discontinuities within A. erythrurus based on a mitochondrial fragment and nine nuclear markers independently. Using the nuclear markers, we then applied linear regression models to investigate whether genetic divergence could be explained by geographical distances alone, or barriers to gene flow (real phylogeographic breaks). Results: A. erythrurus is characterized by an important mitochondrial diversity, with 11 strongly supported phylogeographic lineages with a crown age of 6 Mya. Nuclear markers, however, yielded weak phylogenetic support for these lineages. Using clustering methods based on genotypes at nine nuclear loci, we identified phylogeographic clusters that were partly discordant with the mtDNA lineages. Tests of IBD delimited at least four groups of populations separated by barriers to gene flow, but unambiguous separation of vicariance from IBD remained challenging in several cases. Main conclusions: The genetic diversity of A. erythrurus originates from a mix of IBD and vicariance, which were difficult to distinguish, and resulted in similar levels of mitochondrial differentiation. These results highlight that phylogeographic breaks inferred from mitochondrial data should be further investigated using multi-locus data and explicit testing to rule out alternative processes generating discontinuities in mitochondrial diversity, including IBD. We identified four groups of populations within A. erythrurus, separated by barriers to gene flow, but even using nine independent nuclear makers the power of our approach was limited, and further investigation using genome-wide data will be required to resolve the phylogeographic history of this species.
Type: Research article
CC-BY 4.0
@article{10_24072_pcjournal_301,
author = {Rancilhac, Lo{\"\i}s and Miralles, Aur\'elien and Geniez, Philippe and Mendez-Aranda, Daniel and Beddek, Menad and Brito, Jos\'e Carlos and Leblois, Rapha\"el and Crochet, Pierre-Andr\'e},
title = {Phylogeographic breaks and how to find them: {An} empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal},
journal = {Peer Community Journal},
eid = {e74},
publisher = {Peer Community In},
volume = {3},
year = {2023},
doi = {10.24072/pcjournal.301},
language = {en},
url = {https://peercommunityjournal.org/articles/10.24072/pcjournal.301/}
}
TY - JOUR AU - Rancilhac, Loïs AU - Miralles, Aurélien AU - Geniez, Philippe AU - Mendez-Aranda, Daniel AU - Beddek, Menad AU - Brito, José Carlos AU - Leblois, Raphaël AU - Crochet, Pierre-André TI - Phylogeographic breaks and how to find them: An empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal JO - Peer Community Journal PY - 2023 VL - 3 PB - Peer Community In UR - https://peercommunityjournal.org/articles/10.24072/pcjournal.301/ DO - 10.24072/pcjournal.301 LA - en ID - 10_24072_pcjournal_301 ER -
%0 Journal Article %A Rancilhac, Loïs %A Miralles, Aurélien %A Geniez, Philippe %A Mendez-Aranda, Daniel %A Beddek, Menad %A Brito, José Carlos %A Leblois, Raphaël %A Crochet, Pierre-André %T Phylogeographic breaks and how to find them: An empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal %J Peer Community Journal %D 2023 %V 3 %I Peer Community In %U https://peercommunityjournal.org/articles/10.24072/pcjournal.301/ %R 10.24072/pcjournal.301 %G en %F 10_24072_pcjournal_301
Rancilhac, Loïs; Miralles, Aurélien; Geniez, Philippe; Mendez-Aranda, Daniel; Beddek, Menad; Brito, José Carlos; Leblois, Raphaël; Crochet, Pierre-André. Phylogeographic breaks and how to find them: An empirical attempt at separating vicariance from isolation by distance in a lizard with restricted dispersal. Peer Community Journal, Volume 3 (2023), article no. e74. doi : 10.24072/pcjournal.301. https://peercommunityjournal.org/articles/10.24072/pcjournal.301/
Peer reviewed and recommended by PCI : 10.24072/pci.evolbiol.100634
Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.
[1] Tropical specialist vs. climate generalist: Diversification and demographic history of sister species of Carlia skinks from northwestern Australia, Molecular Ecology, Volume 26 (2017) no. 15, pp. 4045-4058 | DOI
[2] When gaps really are gaps: statistical phylogeography of hydrothermal vent invertebrates, Evolution, Volume 64 (2010), pp. 2369-2384 | DOI
[3] Intraspecific phylogeography: The Mitochondrial DNA Bridge Between Population Genetics and Systematics, Annual Review of Ecology and Systematics, Volume 18 (1987) no. 1, pp. 489-522 | DOI
[4] Comparative phylogeography of amphibians and reptiles in Algeria suggests common causes for the east-west phylogeographic breaks in the Maghreb, PLOS ONE, Volume 13 (2018) no. 8 | DOI
[5] Comparative phylogeography of amphibians and reptiles in Algeria suggests common causes for the east-west phylogeographic breaks in the Maghreb, PLOS ONE, Volume 13 (2018) no. 8 | DOI
[6] GENETIX 4.05, logiciel sous Windows TM pour la génétique des populations, Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier (France), 2004 (https://kimura.univ-montp2.fr/genetix/accessed 03/2023)
[7] Habitat discontinuities form strong barriers to gene flow among mangrove populations, despite the capacity for long-distance dispersal, Diversity and Distributions, Volume 25 (2018) no. 2, pp. 298-309 | DOI
[8] Contribution to the systematics of the lizard Acanthodactylus erythrurus (Sauria, Lacertidae) in Morocco, Herpetological Journal, Volume 5 (1995), pp. 271-280
[9] The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness?, Biological Journal of the Linnean Society, Volume 106 (2012) no. 4, pp. 699-716 | DOI
[10] Multilocus phylogeography and phylogenetics using sequence-based markers, Genetica, Volume 135 (2008) no. 3, pp. 439-455 | DOI
[11] Unravelling biodiversity, evolution and threats to conservation in the Sahara-Sahel, Biological Reviews, Volume 89 (2013) no. 1, pp. 215-231 | DOI
[12] Lack of congruence of genetic and niche divergence in Podarcis hispanicus complex, Journal of Zoological Systematics and Evolutionary Research, Volume 56 (2018) no. 4, pp. 479-492 | DOI
[13] Nuclear phylogenies and genomics of a contact zone establish the species rank of Podarcis lusitanicus (Squamata, Lacertidae), Molecular Phylogenetics and Evolution, Volume 164 (2021) | DOI
[14] Variable levels of introgression between the endangered Podarcis carbonelli and highly divergent congeneric species, Heredity, Volume 126 (2020) no. 3, pp. 463-476 | DOI
[15] Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot, Science, Volume 323 (2009) no. 5915, pp. 785-789 | DOI
[16] Stability Predicts Genetic Diversity in the Brazilian Atlantic Forest Hotspot, Science, Volume 323 (2009) no. 5915, pp. 785-789 | DOI
[17] Iberian hares with anciently introgressed mitochondrial DNA express a marginal environmental niche, Journal of Biogeography, Volume 48 (2021) no. 9, pp. 2328-2336 | DOI
[18] Terrace Aware Data Structure for Phylogenomic Inference from Supermatrices, Systematic Biology, Volume 65 (2016) no. 6, pp. 997-1008 | DOI
[19] Uncovering cryptic diversity and refugial persistence among small mammal lineages across the Eastern Afromontane biodiversity hotspot, Molecular Phylogenetics and Evolution, Volume 71 (2014), pp. 41-54 | DOI
[20] Combining RADseq and contact zone analysis to decipher cryptic diversification in reptiles: insights from Acanthodactylus erythrurus (Reptilia: Lacertidae), Zoologica Scripta, 2023 | DOI
[21] Are glacial refugia hotspots of speciation and cytonuclear discordances? Answers from the genomic phylogeography of Spanish common frogs, Molecular Ecology, Volume 29 (2020) no. 5, pp. 986-1000 | DOI
[22] Integrating hybrid zone analyses in species delimitation: lessons from two anuran radiations of the Western Mediterranean, Heredity, Volume 124 (2020) no. 3, pp. 423-438 | DOI
[23] Shallow phylogeographic histories of key species in a biodiversity hotspot, Phycologia, Volume 54 (2015) no. 6, pp. 556-565 | DOI
[24] Evolutionary history of the two North African hedgehogs (Mammalia: Erinaceidae) Atelerix algirus and Paraechinus aethiopicus based on phylogeography and species distribution modelling, Vertebrate Zoology, Volume 71 (2021), pp. 799-811 | DOI
[25] Congruent signals of population history but radically different patterns of genetic diversity between mitochondrial and nuclear markers in a mountain lizard, Molecular Ecology, Volume 24 (2014) no. 1, pp. 192-207 | DOI
[26] Phylogeography of Psammodromus algirus (Linnaeus, 1758) in Morocco, Herpetology Notes, Volume 13 (2020), pp. 1055-1061
[27] Systematic and phylogeographical assessment of the Acanthodactylus erythrurus group (Reptilia: Lacertidae) based on phylogenetic analyses of mitochondrial and nuclear DNA, Molecular Phylogenetics and Evolution, Volume 51 (2009) no. 2, pp. 131-142 | DOI
[28] Estimating patterns of reptile biodiversity in remote regions, Journal of Biogeography, Volume 40 (2012) no. 6, pp. 1202-1211 | DOI
[29] Using spatial Bayesian methods to determine the genetic structure of a continuously distributed population: clusters or isolation by distance?, Journal of Applied Ecology, Volume 46 (2009) no. 2, pp. 493-505 | DOI
[30] Species-Level Paraphyly and Polyphyly: Frequency, Causes, and Consequences, with Insights from Animal Mitochondrial DNA, Annual Review of Ecology, Evolution, and Systematics, Volume 34 (2003) no. 1, pp. 397-423 | DOI
[31] Environmental temperatures shape thermal physiology as well as diversification and genome-wide substitution rates in lizards, Nature Communications, Volume 10 (2019) no. 1 | DOI
[32] Refugia within Refugia: Patterns of Phylogeographic Concordance in the Iberian Peninsula, Phylogeography of Southern European Refugia, Springer Netherlands, Dordrecht, pp. 155-188 | DOI
[33] Geographic separation and genetic differentiation of populations are not coupled with niche differentiation in threatened Kaiser’s spotted newt (Neurergus kaiseri), Scientific Reports, Volume 9 (2019) no. 1 | DOI
[34] Integrative inference of population history in the Ibero-Maghrebian endemic Pleurodeles waltl (Salamandridae), Molecular Phylogenetics and Evolution, Volume 112 (2017), pp. 122-137 | DOI
[35] Species delimitation and geography, Molecular Ecology Resources, Volume 20 (2020) no. 4, pp. 950-960 | DOI
[36] Bayesian Inference of Species Trees from Multilocus Data, Molecular Biology and Evolution, Volume 27 (2010) no. 3, pp. 570-580 | DOI
[37] Is population subdivision different from speciation? From phylogeography to species delimitation, Ecology and Evolution, Volume 10 (2020) no. 14, pp. 6890-6896 | DOI
[38] Palaearctic biogeography revisited: evidence for the existence of a North African refugium for Western Palaearctic biota, Journal of Biogeography, Volume 41 (2013) no. 1, pp. 81-94 | DOI
[39] Phylogeographic breaks without geographic barriers to gene flow, Evolution, Volume 56 (2002) no. 12 | DOI
[40] Local Adaptation along Smooth Ecological Gradients Causes Phylogeographic Breaks and Phenotypic Clustering, The American Naturalist, Volume 180 (2012) no. 1, pp. 35-49 | DOI
[41] Phylogeography of western Palaearctic reptiles – Spatial and temporal speciation patterns, Zoologischer Anzeiger - A Journal of Comparative Zoology, Volume 246 (2007) no. 4, pp. 293-313 | DOI
[42] adegenet: a R package for the multivariate analysis of genetic markers, Bioinformatics, Volume 24 (2008) no. 11, pp. 1403-1405 | DOI
[43] ModelFinder: fast model selection for accurate phylogenetic estimates, Nature Methods, Volume 14 (2017) no. 6, pp. 587-589 | DOI
[44] Molecular biogeography of the Mediterranean Buthus species complex (Scorpiones: Buthidae) at its southern Palaearctic margin, Biological Journal of the Linnean Society, Volume 133 (2021) no. 1, pp. 166-178 | DOI
[45] Statistical Phylogeography, Annual Review of Ecology, Evolution, and Systematics, Volume 40 (2009) no. 1, pp. 593-612 | DOI
[46] A review of phylogeography: biotic and abiotic factors, Geology, Ecology, and Landscapes, Volume 2 (2018) no. 4, pp. 268-274 | DOI
[47] Phylogeographic breaks in low-dispersal species: the emergence of concordance across gene trees, Genetica, Volume 124 (2005) no. 2-3, pp. 179-186 | DOI
[48] Comparative phylogeography of West African amphibians and reptiles, Evolution, Volume 74 (2020) no. 4, pp. 716-724 | DOI
[49] Climate, flora and fauna changes in the Sahara over the past 500 million years, Journal of Arid Environments, Volume 37 (1997) no. 4, pp. 619-647 | DOI
[50] DnaSP v5: a software for comprehensive analysis of DNA polymorphism data, Bioinformatics, Volume 25 (2009) no. 11, pp. 1451-1452 | DOI
[51] Morphology and multilocus phylogeny of the Spiny-footed Lizard (Acanthodactylus erythrurus) complex reveal two new mountain species from the Moroccan Atlas, Zootaxa, Volume 4747 (2020) no. 2 | DOI
[52] IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies, Molecular Biology and Evolution, Volume 32 (2014) no. 1, pp. 268-274 | DOI
[53] Phylogeography and ecological niche modeling unravel the evolutionary history of the African green toad, Bufotes boulengeri boulengeri (Amphibia: Bufonidae), through the Quaternary, Journal of Zoological Systematics and Evolutionary Research, Volume 56 (2017) no. 1, pp. 102-116 | DOI
[54] Contrasting population structure from nuclear intron sequences and mtDNA of humpback whales., Molecular Biology and Evolution, Volume 11 (1994), pp. 426-435 | DOI
[55] Relationships between gene trees and species trees., Molecular Biology and Evolution, Volume 5 (1988), pp. 568-583 | DOI
[56] The difficult task of partitioning the effects of vicariance and isolation by distance in poor dispersers, Peer Community in Evolutionary Biology (2023) | DOI
[57] ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R, Bioinformatics, Volume 35 (2018) no. 3, pp. 526-528 | DOI
[58] Assessing population structure in the face of isolation by distance: Are we neglecting the problem?, Diversity and Distributions, Volume 24 (2018) no. 12, pp. 1883-1889 | DOI
[59] Visualizing spatial population structure with estimated effective migration surfaces, Nature Genetics, Volume 48 (2015) no. 1, pp. 94-100 | DOI
[60] Contrasting scales of local persistence between monsoonal and arid biomes in closely related, low‐dispersal vertebrates, Journal of Biogeography, Volume 46 (2019) no. 11, pp. 2506-2519 | DOI
[61] Inference of Population Structure Using Multilocus Genotype Data, Genetics, Volume 155 (2000) no. 2, pp. 945-959 | DOI
[62] rancilhac/IBD_vs_Vicariance: Data and scripts for Rancilhac et al. 2023 (https://doi.org/10.1101/2022.09.30.510256) (v1.0), Zenodo, 2022 | DOI
[63] Support from the relationship of genetic and geographic distance in human populations for a serial founder effect originating in Africa, Proceedings of the National Academy of Sciences, Volume 102 (2005) no. 44, pp. 15942-15947 | DOI
[64] Morphology and nuclear markers reveal extensive mitochondrial introgressions in the Iberian Wall Lizard species complex, Molecular Ecology, Volume 18 (2009) no. 20, pp. 4298-4315 | DOI
[65] Evolutionary History of the Morocco lizard-Fingered Geckos of the Saurodactylus brosseti Complex, Evolutionary Biology, Volume 44 (2017) no. 3, pp. 386-400 | DOI
[66] Genetic Differentiation and Estimation of Gene Flow from F-Statistics Under Isolation by Distance, Genetics, Volume 145 (1997) no. 4, pp. 1219-1228 | DOI
[67] genepop’007: a complete re-implementation of the genepop software for Windows and Linux, Molecular Ecology Resources, Volume 8 (2008) no. 1, pp. 103-106 | DOI
[68] A revision of the lizards of the genus Acanthodactylus (Sauria: Lacertidae)., Bonner Zoologisches Monographien, Nr. 16, Zoologisches Forschungsinstitut und Museum Alexander Koenig (1982), pp. 1-167
[69] Digging up the roots of an insular hotspot of genetic diversity: decoupled mito-nuclear histories in the evolution of the Corsican-Sardinian endemic lizard Podarcis tiliguerta, BMC Evolutionary Biology, Volume 17 (2017) no. 1 | DOI
[70] Fossil-calibrated time tree of Podarcis wall lizards provides limited support for biogeographic calibration models, Molecular Phylogenetics and Evolution, Volume 161 (2021) | DOI
[71] Evidence for Gradients of Human Genetic Diversity Within and Among Continents, Genome Research, Volume 14 (2004) no. 9, pp. 1679-1685 | DOI
[72] Conservation Genetics and Genomics of Amphibians and Reptiles, Annual Review of Animal Biosciences, Volume 3 (2015) no. 1, pp. 113-138 | DOI
[73] Mitochondrial ghost lineages blur phylogeography and taxonomy of Natrix helvetica and N. natrix in Italy and Corsica, Zoologica Scripta, Volume 49 (2020) no. 4, pp. 395-411 | DOI
[74] Why sampling scheme matters: the effect of sampling scheme on landscape genetic results, Conservation Genetics, Volume 10 (2008) no. 2, pp. 441-452 | DOI
[75] Out of Africa: Phylogeny and biogeography of the widespread genus Acanthodactylus (Reptilia: Lacertidae), Molecular Phylogenetics and Evolution, Volume 103 (2016), pp. 6-18 | DOI
[76] MEGA11: Molecular Evolutionary Genetics Analysis Version 11, Molecular Biology and Evolution, Volume 38 (2021) no. 7, pp. 3022-3027 | DOI
[77] Mitochondrial DNA is unsuitable to test for isolation by distance, Scientific Reports, Volume 8 (2018) no. 1 | DOI
[78] The biogeography of mitochondrial and nuclear discordance in animals, Molecular Ecology, Volume 21 (2012) no. 16, pp. 3907-3930 | DOI
[79] Taxonomic inflation due to inadequate sampling: are girdled lizards (Cordylus minor species complex) from the Great Karoo one and the same?, Biological Journal of the Linnean Society, Volume 135 (2021) no. 1, pp. 1-24 | DOI
[80] Living on the edge: Ecological and genetic connectivity of the spiny-footed lizard,Acanthodactylus aureus, confirms the Atlantic Sahara desert as a biogeographic corridor and centre of lineage diversification, Journal of Biogeography, Volume 45 (2018) no. 5, pp. 1031-1042 | DOI
[81] Pleistocene diversification in Morocco and recent demographic expansion in the Mediterranean pond turtle Mauremys leprosa, Biological Journal of the Linnean Society, Volume 119 (2016) no. 4, pp. 943-959 | DOI
[82] Does the DNA barcoding gap exist? – a case study in blue butterflies (Lepidoptera: Lycaenidae), Frontiers in Zoology, Volume 4 (2007) no. 1 | DOI
[83] No evidence for nuclear introgression despite complete mtDNA replacement in the Carpathian newt (Lissotriton montandoni), Molecular Ecology, Volume 22 (2013) no. 7, pp. 1884-1903 | DOI
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