Archipelagic genetics in a widespread Caribbean anole

R.G. Reynolds; T.R. Strickland; J.J. Kolbe; B.G. Falk; G. Perry; L.J. Revell; J.B. Losos

doi:10.1111/jbi.13072

Archipelagic genetics in a widespread Caribbean anole

R.G. Reynolds, T.R. Strickland, J.J. Kolbe, B.G. Falk, G. Perry, L.J. Revell, J.B. Losos

Research output: Contribution to journal › Research Article › peer-review

15 Scopus citations

Abstract

Aim: We examine the influence of fluctuating sea levels in a land-bridge archipelago on the apportioning of intraspecific genetic diversity and divergence in the widespread Puerto Rican crested anole (Anolis cristatellus). We compare three alternative scenarios for genetic diversification in an archipelagic species that contrast the relative influences of periodic isolation versus island connectedness driven by fluctuating sea levels. Our approach combines information from geography and population genetics to assess the influence of island size, island isolation, island historical geography, and population genetic processes such as drift on the contemporary distribution of genetic variation within and among islands. Location: The Puerto Rico Bank in the Caribbean focusing primarily on the Spanish, British and U.S. Virgin Islands. Methods: We used nuclear and mitochondrial DNA sequences and microsatellite genotypes sampled from A. cristatellus populations to investigate: (1) the broad-scale pattern of phylogeographical divergence across Puerto Rico Bank islands and (2) diversification within the Virgin Islands archipelago. For the first component, we used sequence data to reconstruct the relationships among 542 samples from across the species range. For the second component, we examined the relative influences of island size, isolation, and population genetic processes on the distribution of genetic diversity across the Virgin Islands. Results: In the Virgin Islands, A. cristatellus is represented by a monophyletic clade except on the island of Vieques, where two divergent clades coexist. We found evidence for non-equilibrium dynamics in the Virgin Islands, suggesting spatial population expansion during intraglacial periods of low sea level. Main conclusions: We found limited evidence that periods of island isolation affected patterns of genetic diversity and differentiation. Instead, we found that the patterns of genetic diversity and divergence in A. cristatellus in the Virgin Islands archipelago are likely shaped by long-term persistence in the region and periods of population spatial expansion. © 2017 John Wiley & Sons Ltd

Original language	English (US)
Pages (from-to)	2631-2647
Number of pages	17
Journal	Journal of Biogeography
Volume	44
Issue number	11
DOIs	https://doi.org/10.1111/jbi.13072
State	Published - 2017
Externally published	Yes

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@article{31022cc5c2f74cf39170cb4279437bdb,

title = "Archipelagic genetics in a widespread Caribbean anole",

abstract = "Aim: We examine the influence of fluctuating sea levels in a land-bridge archipelago on the apportioning of intraspecific genetic diversity and divergence in the widespread Puerto Rican crested anole (Anolis cristatellus). We compare three alternative scenarios for genetic diversification in an archipelagic species that contrast the relative influences of periodic isolation versus island connectedness driven by fluctuating sea levels. Our approach combines information from geography and population genetics to assess the influence of island size, island isolation, island historical geography, and population genetic processes such as drift on the contemporary distribution of genetic variation within and among islands. Location: The Puerto Rico Bank in the Caribbean focusing primarily on the Spanish, British and U.S. Virgin Islands. Methods: We used nuclear and mitochondrial DNA sequences and microsatellite genotypes sampled from A. cristatellus populations to investigate: (1) the broad-scale pattern of phylogeographical divergence across Puerto Rico Bank islands and (2) diversification within the Virgin Islands archipelago. For the first component, we used sequence data to reconstruct the relationships among 542 samples from across the species range. For the second component, we examined the relative influences of island size, isolation, and population genetic processes on the distribution of genetic diversity across the Virgin Islands. Results: In the Virgin Islands, A. cristatellus is represented by a monophyletic clade except on the island of Vieques, where two divergent clades coexist. We found evidence for non-equilibrium dynamics in the Virgin Islands, suggesting spatial population expansion during intraglacial periods of low sea level. Main conclusions: We found limited evidence that periods of island isolation affected patterns of genetic diversity and differentiation. Instead, we found that the patterns of genetic diversity and divergence in A. cristatellus in the Virgin Islands archipelago are likely shaped by long-term persistence in the region and periods of population spatial expansion. {\textcopyright} 2017 John Wiley & Sons Ltd",

author = "R.G. Reynolds and T.R. Strickland and J.J. Kolbe and B.G. Falk and G. Perry and L.J. Revell and J.B. Losos",

note = "Export Date: 17 April 2018 CODEN: JBIOD Correspondence Address: Reynolds, R.G.; Department of Biology, University of North Carolina AshevilleUnited States; email: [email protected] Funding details: University of Massachusetts Boston Funding details: 1-4 Funding details: 2012-IC-049 Funding details: 2012001 Funding details: URI, University of Rhode Island Funding details: STT034-10 Funding details: Harvard University Funding details: MCZ, Museum of Comparative Zoology, Harvard University Funding details: 26-11 Funding details: UC Berkeley, University of California Berkeley Funding text: We are grateful to the Puerto Rico Departamento de Recursos Natu-rales y Ambientales (DRNA) for permits and assistance. All samples were collected under DRNA permits 2011-IC-041 (to B.G.F.) and 2012-IC-049 (to L.J.R.); USFW permits STT034-10 (to B.G.F.); and from the Turks and Caicos Dept. of Environment and Coastal Resources #1-4 (to R.G.R.). We thank Ian Wang (UC Berkeley) and Kristin Winchell (UMass Boston) for graciously providing some samples from the main island of Puerto Rico and Haley Moniz (URI) for excellent advice regarding microsatellite protocols. We are also grateful to Ellen Lapuck (UMass Boston) for laboratory assistance, Alberto R. Puente-Rol{\'o}n (UPR Mayaguez) for assistance with permitting, logistics, and help in the field, as well as to local landowners in Puerto Rico and the Virgin Islands for property access. We are grateful for funding from the Harvard Herchel-Smith Summer Undergraduate Research Program and from the Harvard Museum of Comparative Zoology Grant-in-Aid of Undergraduate Research Program (both to T.R.S.). We also acknowledge support from the University of Massachusetts Boston, Harvard University, the Harvard Museum of Comparative Zoology, the University of Rhode Island, and the Falconwood Foundation through a grant to The Conservation Agency. Portions of this work have been approved by the University of Massachusetts Boston Institutional Animal Care and Use Committee (IACUC) Protocol #2012001 and the Harvard University IACUC Protocol # 26-11. We thank Benjamin Fitzpatrick, Travis Ingram, and Gabriel Gartner for advice related to this work, as well as the Losos Lab at Harvard and the Revell Lab at UMass Boston for advice and comments on this project. We thank the Chief Editor Bradford Hawkins, Editor Robert Bryson Jr., and four anonymous reviewers for helpful and important comments and suggestions on previous versions of this manuscript. References: Barker, B.S., Rodr{\'i}guez-Robles, J.A., Aran, V.S., Montoya, A., Waide, R.B., Cook, J.A., Sea level, topography and island diversity: Phylogeography of the Puerto Rican Red–eyed Coqu{\'i}, Eleutherodactylus antillensis (2012) Molecular Ecology, 21, pp. 6033-6052; Bitanja, R., van de Wal, R.S.W., Oerlemans, J., Modelled atmospheric temperatures and global sea levels over the past million years (2005) Nature, 437, pp. 125-128; Brandley, M.C., de Quieroz, K., Phylogeny, ecomorphological evolution, and historical biogeography of the Anolis cristatellus series (2004) Herpetological Monographs, 18, pp. 90-126; C{\'a}diz, A., Nagata, N., Katabuchi, M., D{\'i}az, L.M., Echeniqu-D{\'i}az, L.M., Akashi, H.D., Kawata, M., Relative importance of habitat use, range expansion, and speciation in local species diversity of Anolis lizards in Cuba (2013) Ecosphere, 4, pp. 1-33; Chapuis, M.-P., Estoup, A., Microsatellite null alleles and estimation of population differentiation (2007) Molecular Biology and Evolution, 24, pp. 621-631; Cornuet, J.M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M., Leblois, R., Estoup, A., DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history suing single nucleotide polymorphism, DNA sequence and microsatellite data (2014) Bioinformatics, 30, pp. 1187-1189; Darriba, D., Taboada, G.L., Doallo, R., Posada, D., jModelTest 2: More models, new heuristics and parallel computing (2012) Nature Methods, 9, p. 772; Degnan, J.H., Rosenberg, N.A., Gene tree discordance, phylogenetic inference and the multispecies coalescent (2009) Trends in Ecology and Evolution, 24, pp. 332-340; Donn, W.L., Farrand, W.R., Ewing, M., Pleistocene ice volumes and sea–level lowering (1962) Journal of Geology, 70, pp. 206-214; Drummond, A.J., Rambaut, A., Shapiro, B., Pybus, O.G., Bayesian coalescent inference of past population dynamics from molecular sequences (2005) Molecular Biology and Evolution, 22, pp. 1185-1192; Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., Bayesian phylogenetics with BEAUTi and the BEAST 1.7 (2012) Molecular Biology and Evolution, 29, pp. 1969-1973; Dutton, A., Bard, E., Antonioli, F., Esat, T.M., Lambeck, K., McCulloch, M.T., Phasing and amplitude of sea–level and climate change during the penultimate interglacial (2009) Nature Geoscience, 2, pp. 355-359; Eales, J., Thorpe, R.S., Malhotra, A., Colonization history and genetic diversity: Adaptive potential in early stage invasions (2010) Molecular Ecology, 19, pp. 2858-2869; Edgar, R.C., MUSCLE: A multiple sequence alignment method with reduced time and space complexity (2004) BMC Bioinformatics, 5, p. 113; Edwards, S.V., Liu, L., Pearl, D.K., High-resolution species trees without concatenation (2007) Proceedings of the National Academy of Sciences USA, 104, pp. 5936-5941; Ersts, P.J., (2014) Geographic Distance Matrix Generator (version 1.2.3), , http://biodiversityinformatics.amnh.org/open_source/gdmg, . [Internet], American Museum of Natural History, Center for Biodiversity and Conservation. Retrieved from, Accessed 5 May 2014; Excoffier, L., Patterns of DNA sequence diversity and genetic structure after a range expansion: Lessons from the infinite–island model (2004) Molecular Ecology, 13, pp. 853-864; Excoffier, L., Lischer, H.E.L., Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows (2010) Molecular Ecology Resources, 10, pp. 564-567; Excoffier, L., Smouse, P., Quattro, J., Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data (1992) Genetics, 131, pp. 479-491; Fairbanks, R.G., A 17,000–year glacio–eustatic sea level record: Influence of glacial melting rates on the Younger Dryas event and deep–ocean circulation (1989) Nature, 342, pp. 637-641; Falk, B.G., Perkins, S.L., Host specificity shapes population structure of pinworm parasites in Caribbean reptiles (2013) Molecular Ecology, 22, pp. 4576-4590; Faubet, P., Waples, R.S., Gaggiotti, O.E., Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates (2007) Molecular Ecology, 16, pp. 1149-1166; Felsenstein, J., (2004) Inferring phylogenies, , Sunderland, Sinauer Associates; Finn, D.S., Bogan, M.T., Lytle, D.A., Demographic stability metrics for conservation prioritization of isolated populations (2009) Conservation Biology, 23, pp. 1185-1194; Gartner, G.E.A., Gamble, T., Jaffe, A., Harrison, A., Losos, J.B., Left–right dewlap asymmetry and phylogeography of Anolis lineatus on Aruba and Cura{\c c}ao (2013) Biological Journal of the Linnean Society, 110, pp. 409-426; Geneva, A.J., Hilton, J., Noll, S., Glor, R.E., Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group) (2015) Molecular Phylogenetics and Evolution, 87, pp. 105-117; Glor, R.E., Johnson, M.A., Larson, A., Polymorphic microsatellite loci for the Puerto Rican crested anole (Anolis cristatellus) and their amplification in related Puerto Rican species (2007) Conservation Genetics, 8, pp. 1491-1493; Goldstein, D.B., Pollock, D.D., Launching microsatellites: A review of mutation processes and method for phylogenetic inference (1997) Journal of Heredity, 88, pp. 335-342; Guindon, S., Gascuel, O., A simple, fast and accurate method to estimate large phylogenies by maximum–likelihood (2003) Systematic Biology, 52, pp. 696-704; Gustafson, E.J., Parker, G.R., Relationships between landcover proportion and indices of landscape spatial pattern (1992) Landscape Ecology, 7, pp. 101-110; Hardy, O.J., Charbonnel, N., Fr{\'e}ville, H., Heuertz, M., Microsatellite allele sizes: A simple test to assess their significance on genetic differentiation (2003) Genetics, 163, pp. 1467-1482; Harmon, L.J., Schulte, J.A., II, Larson, A., Losos, J.B., Tempo and mode of evolutionary radiation in iguanian lizards (2003) Science, 301, pp. 961-964; Hearty, P.J., Hollin, J.T., Neumann, A.C., O'Leary, M.J., McCulloch, M., Global sea–level fluctuations during the Last Interglaciation (MIS 5e) (2007) Quaternary Science Reviews, 26, pp. 2090-2112; Heatwole, H., Levins, R., Biogeography of the Puerto Rico Bank: Species–turnover on a small cay, Cayo Ahogado (1973) Ecology, 54, pp. 1042-1055; Heatwole, H., MacKenzie, F., Herpetogeography of Puerto Rico. IV. Paleogeography, faunal similarity an endemism (1967) Evolution, 21, pp. 429-438; Hedrick, P.W., (2009) Genetics of populations, , 4th ed., Sudbury, MA, Jones and Bartlett; Heled, J., Drummond, A.J., Bayesian inference of species trees from multilocus data (2010) Molecular Biology and Evolution, 27, pp. 570-580; Hertz, P.E., Eurythermy and niche breadth in West Indian Anolis lizards: A reappraisal (1983) Advances in herpetology and evolutionary biology, pp. 472-483. , In, A. G. J. Rhodin, #x0026;, K. Miyata, (Eds.),, Cambridge, Museum of Comparative Zoology; Ho, S.Y.W., Phillips, M.J., Cooper, A., Drummond, A.J., Time dependency of molecular rate estimates and systematic overestimation of recent divergence times (2005) Molecular Biology and Evolution, 22, pp. 1561-1568; Huson, D.H., Bryant, D., Application of phylogenetic networks in evolutionary studies (2006) Molecular Biology and Evolution, 23, pp. 254-267; Johnson, K.P., Adler, F.R., Cherry, J.L., Genetic and phylogenetic consequences of island biogeography (2000) Evolution, 52, pp. 387-396; Jombart, T., Adegenet: A R package for the multivariate analysis of genetic markers (2008) Bioinformatics, 24, pp. 1403-1405; Jombart, T., Devillard, S., Balloux, F., Discriminant analysis of principal components: A new method for the analysis genetically structured populations (2010) BMC Genetics, 11, p. 94; Karl, S.A., Toonen, R.J., Grant, W.S., Bowen, B.W., Common misconceptions in molecular ecology: Echoes of the modern synthesis (2012) Molecular Ecology, 21, pp. 4171-4189; Keenan, K., McGinnity, P., Cross, T.R., Crozier, W.W., Prod{\"o}hl, P., DiveRsity: An R package for the estimation and exploration of population genetic parameters and their associated errors (2013) Methods in Ecology and Evolution, 4, pp. 782-788; Kolbe, J.J., Glor, R.E., Rodr{\'i}guez-Schettino, L., Lara, A.C., Larson, A., Losos, J.B., Genetic variation increases during biological invasion by a Cuban lizard (2004) Nature, 431, pp. 177-181; Kolbe, J.J., Larson, A., Losos, J.B., Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei (2007) Molecular Ecology, 16, pp. 1579-1591; Lanfear, R., Welch, J.J., Bromham, L., Watching the clock: Studying rates of molecular evolution between species (2010) Trends in Ecology and Evolution, 25, pp. 495-503; Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Higgins, D.G., Clustal W and Clustal X version 2.0 (2007) Bioinformatics, 23, pp. 947-2948; Librado, P., Rozas, J., DnaSP v5: A software for comprehensive analysis of DNA polymorphism data (2009) Bioinformatics, 25, pp. 1451-1452; Lighty, R.G., Macintyre, I.G., Stuckenrath, R., Acropora palmata reef framework: A reliable indicator of sea level in the Western Atlantic for the past 10,000 years (1982) Coral Reefs, 1, pp. 125-130; Loew, S.S., Williams, D.F., Ralls, K., Pilgrim, K., Fleischer, R.C., Population structure and genetic variation in the endangered giant kangaroo rat (Dipodomys ingens) (2005) Conservation Genetics, 6, pp. 495-510; Losos, J.B., Ricklefs, R.E., Adaptation and diversification on islands (2009) Nature, 457, pp. 830-836; Macey, J.R., Schulte, J.A., II, Ananjeva, N.B., Larson, A., Rastegar-Pouyani, N., Shammakov, S.M., Papenfuss, T.J., Phylogenetic relationships among agamid lizards of the Laudakia caucasia species group: Testing hypotheses of biogeographic fragmentation and an area cladogram for the Iranian Plateau (1998) Molecular Phylogenetics and Evolution, 10, pp. 118-131; Mantel, N.A., The detection of disease clustering and a generalized regression approach (1967) Cancer Research, 27, pp. 209-220; Mayer, G.C., Island lists of West Indian amphibians and reptiles (2012) Bulletin of the Florida Museum of Natural History, 51, pp. 85-166. , . Puerto Rico and the Virgin Islands. In, R. Powell, &, R. W. Henderson, (Eds.); Meiri, S., Oceanic island biogeography: Nomothetic science of the anecdotal (2017) Frontiers of Biogeography, 9 (1); Meirmans, P.G., The trouble with isolation by distance (2012) Molecular Ecology, 21, pp. 2839-2846; Meirmans, P.G., Nonconvergence in Bayesian estimation of migration rates (2014) Molecular Ecology Resources, 14, pp. 726-733; Pannell, J.R., Coalescence in a metapopulation with recurrent local extinction and recolonization (2003) Evolution, 57, pp. 949-961; Papadopoulou, A., Knowles, L.L., Genomic tests of the species-pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands (2015) Evolution, 69, pp. 1501-1517; Peakall, R., Smouse, P.E., Genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research (2006) Molecular Ecology Notes, 6, pp. 288-295; Perry, G., Powell, R., Watson, H., Keeping invasive species off Guana Island, British Virgin Islands (2006) Iguana: Conservation Natural History, and Husbandry of Reptiles, 13, pp. 273-277; Peterson, G.I., Masel, J., Quantitative prediction of molecular clock and Ka/Ks at short timescales (2009) Molecular Biology and Evolution, 26, pp. 2595-2603; (2016) R: A language and environment for statistical computing, , https://www.R-project.org, Vienna, Austria, R Foundation for Statistical Computing, Retrieved from; Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., (2013) Tracer v1.5, , http://beast.bio.ed.ac.uk/Tracer, #x0026;, Retrieved from; Raymond, M., Rousset, F., GenePop v1.2: Population genetics software for exact test and ecumenicism (1995) Journal of Heredity, 86, pp. 248-249; Revell, L.J., Harmon, L.J., Langerhans, R.B., Kolbe, J.J., A phylogenetic approach to determining the importance of constraint on phenotypic evolution in the neotropical lizard Anolis cristatellus (2007) Evolutionary Ecology Research, 9, pp. 261-282; Reynolds, R.G., Niemiller, M.L., Hedges, S.B., Dornburg, A., Puente-Rol{\'o}n, A.R., Revell, L.J., Molecular phylogeny and historical biogeography of West Indian boid snakes (Chilabothrus) (2013) Molecular Phylogenetics and Evolution, 68, pp. 461-470; Rodr{\'i}guez-Robles, J.A., Jezkova, T., Garc{\'i}a, M.A., Evolutionary relationships and historical biogeography of Anolis desechensis and Anolis monensis, two lizards endemic to small islands in the eastern Caribbean Sea (2007) Journal of Biogeography, 34, pp. 1546-1558; Rogers, A.R., Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences (1992) Molecular Biology and Evolution, 9, pp. 552-569; Rohling, E.J., Grant, K., Bolshaw, M., Roberts, A.P., Siddall, M., Hemleben, C., Kucera, M., Antarctic temperature and global sea level closely coupled over the past five glacial cycles (2009) Nature Geoscience, 2, pp. 500-504; Rousset, F., Genetic differentiation and estimation of gene flow from F–statistics under isolation by distance (1997) Genetics, 145, pp. 1219-1228; Samarasin, P., Shuter, B.J., Wright, S.I., Rodd, F.H., The problem of estimating recent genetic connectivity in a changing world (2016) Conservation Biology, 31, pp. 126-135; Schuelke, M., An economic method for the fluorescent labelling of PCR fragments (2000) Nature Biotechnology, 18, pp. 233-234; Siddall, M., Rohling, E.J., Almogi-Labin, A., Hemleben, C., Meischner, D., Schmelzer, I., Smeed, D.A., Sea–level fluctuations during the last glacial cycle (2003) Nature, 423, pp. 854-858; Slatkin, M., Gene flow and the geographic structure of natural populations (1987) Science, 236, pp. 787-792; Slatkin, M., Hudson, R.R., Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations (1991) Genetics, 129, pp. 555-562; Stamatakis, A., RaxML–VI–HPC: Maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models (2006) Bioinformatics, 22, pp. 2688-2690; Stephens, M., Donnelly, P., A comparison of Bayesian methods for haplotype reconstruction from population genotype data (2003) American Journal of Human Genetics, 73, pp. 1162-1169; Stephens, M., Smith, N.J., Donnelly, P., A new statistical method for haplotype reconstruction from population data (2001) American Journal of Human Genetics, 68, pp. 978-989; Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0 (2013) Molecular Evolutionary Biology, 30, pp. 2725-2729; Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data (2004) Molecular Ecology Notes, 4, pp. 535-538; Vellend, M., Island biogeography of genes and species (2003) The American Naturalist, 162, pp. 358-365; Volkmann, L., Martyn, I., Moulton, V., Spillner, A., Mooers, A.O., Prioritizing populations for conservation using phylogenetic networks (2014) PLoS ONE, 9; Wade, M.J., McCauley, D.E., Extinction and recolonization: Their effects on the genetic differentiation of local populations (1988) Evolution, 42, pp. 995-1005; Whitlock, M.C., McCauley, D.E., Some population genetic consequences of colony formation and extinction: Genetic correlations within founding groups (1990) Evolution, 44, pp. 1717-1724; Whitlock, R., (2004) The consequences of genetic impoverishment for plant community structure and function, , PhD Thesis, University of Sheffield, Sheffield; Williams, E.E., The ecology of colonization as seen in the zoogeography of anoline lizards on small islands (1969) The Quarterly Review of Biology, 44, pp. 345-389; Wilson, G., Rannala, B., Bayesian inference of recent migration rates using multilocus genotypes (2003) Genetics, 163, pp. 1177-1191; Wordley, C., Slate, J., Stapley, J., Mining online genomic resources in Anolis carolinensis facilitates rapid and inexpensive development of cross–species microsatellite markers for the Anolis lizard genus (2011) Molecular Ecology Resources, 11, pp. 126-133; Wright, S., Isolation by distance (1943) Genetics, 28, pp. 114-138; Wright, S., (1977) Evolution and the genetics of populations, volume 3: Experimental results and evolutionary deductions, , Chicago, University of Chicago Press",

year = "2017",

doi = "10.1111/jbi.13072",

language = "English (US)",

volume = "44",

pages = "2631--2647",

journal = "Journal of Biogeography",

issn = "0305-0270",

publisher = "Wiley-Blackwell Publishing Ltd",

number = "11",

}

TY - JOUR

T1 - Archipelagic genetics in a widespread Caribbean anole

AU - Reynolds, R.G.

AU - Strickland, T.R.

AU - Kolbe, J.J.

AU - Falk, B.G.

AU - Perry, G.

AU - Revell, L.J.

AU - Losos, J.B.

N1 - Export Date: 17 April 2018 CODEN: JBIOD Correspondence Address: Reynolds, R.G.; Department of Biology, University of North Carolina AshevilleUnited States; email: [email protected] Funding details: University of Massachusetts Boston Funding details: 1-4 Funding details: 2012-IC-049 Funding details: 2012001 Funding details: URI, University of Rhode Island Funding details: STT034-10 Funding details: Harvard University Funding details: MCZ, Museum of Comparative Zoology, Harvard University Funding details: 26-11 Funding details: UC Berkeley, University of California Berkeley Funding text: We are grateful to the Puerto Rico Departamento de Recursos Natu-rales y Ambientales (DRNA) for permits and assistance. All samples were collected under DRNA permits 2011-IC-041 (to B.G.F.) and 2012-IC-049 (to L.J.R.); USFW permits STT034-10 (to B.G.F.); and from the Turks and Caicos Dept. of Environment and Coastal Resources #1-4 (to R.G.R.). We thank Ian Wang (UC Berkeley) and Kristin Winchell (UMass Boston) for graciously providing some samples from the main island of Puerto Rico and Haley Moniz (URI) for excellent advice regarding microsatellite protocols. We are also grateful to Ellen Lapuck (UMass Boston) for laboratory assistance, Alberto R. Puente-Rolón (UPR Mayaguez) for assistance with permitting, logistics, and help in the field, as well as to local landowners in Puerto Rico and the Virgin Islands for property access. We are grateful for funding from the Harvard Herchel-Smith Summer Undergraduate Research Program and from the Harvard Museum of Comparative Zoology Grant-in-Aid of Undergraduate Research Program (both to T.R.S.). We also acknowledge support from the University of Massachusetts Boston, Harvard University, the Harvard Museum of Comparative Zoology, the University of Rhode Island, and the Falconwood Foundation through a grant to The Conservation Agency. Portions of this work have been approved by the University of Massachusetts Boston Institutional Animal Care and Use Committee (IACUC) Protocol #2012001 and the Harvard University IACUC Protocol # 26-11. We thank Benjamin Fitzpatrick, Travis Ingram, and Gabriel Gartner for advice related to this work, as well as the Losos Lab at Harvard and the Revell Lab at UMass Boston for advice and comments on this project. We thank the Chief Editor Bradford Hawkins, Editor Robert Bryson Jr., and four anonymous reviewers for helpful and important comments and suggestions on previous versions of this manuscript. References: Barker, B.S., Rodríguez-Robles, J.A., Aran, V.S., Montoya, A., Waide, R.B., Cook, J.A., Sea level, topography and island diversity: Phylogeography of the Puerto Rican Red–eyed Coquí, Eleutherodactylus antillensis (2012) Molecular Ecology, 21, pp. 6033-6052; Bitanja, R., van de Wal, R.S.W., Oerlemans, J., Modelled atmospheric temperatures and global sea levels over the past million years (2005) Nature, 437, pp. 125-128; Brandley, M.C., de Quieroz, K., Phylogeny, ecomorphological evolution, and historical biogeography of the Anolis cristatellus series (2004) Herpetological Monographs, 18, pp. 90-126; Cádiz, A., Nagata, N., Katabuchi, M., Díaz, L.M., Echeniqu-Díaz, L.M., Akashi, H.D., Kawata, M., Relative importance of habitat use, range expansion, and speciation in local species diversity of Anolis lizards in Cuba (2013) Ecosphere, 4, pp. 1-33; Chapuis, M.-P., Estoup, A., Microsatellite null alleles and estimation of population differentiation (2007) Molecular Biology and Evolution, 24, pp. 621-631; Cornuet, J.M., Pudlo, P., Veyssier, J., Dehne-Garcia, A., Gautier, M., Leblois, R., Estoup, A., DIYABC v2.0: A software to make approximate Bayesian computation inferences about population history suing single nucleotide polymorphism, DNA sequence and microsatellite data (2014) Bioinformatics, 30, pp. 1187-1189; Darriba, D., Taboada, G.L., Doallo, R., Posada, D., jModelTest 2: More models, new heuristics and parallel computing (2012) Nature Methods, 9, p. 772; Degnan, J.H., Rosenberg, N.A., Gene tree discordance, phylogenetic inference and the multispecies coalescent (2009) Trends in Ecology and Evolution, 24, pp. 332-340; Donn, W.L., Farrand, W.R., Ewing, M., Pleistocene ice volumes and sea–level lowering (1962) Journal of Geology, 70, pp. 206-214; Drummond, A.J., Rambaut, A., Shapiro, B., Pybus, O.G., Bayesian coalescent inference of past population dynamics from molecular sequences (2005) Molecular Biology and Evolution, 22, pp. 1185-1192; Drummond, A.J., Suchard, M.A., Xie, D., Rambaut, A., Bayesian phylogenetics with BEAUTi and the BEAST 1.7 (2012) Molecular Biology and Evolution, 29, pp. 1969-1973; Dutton, A., Bard, E., Antonioli, F., Esat, T.M., Lambeck, K., McCulloch, M.T., Phasing and amplitude of sea–level and climate change during the penultimate interglacial (2009) Nature Geoscience, 2, pp. 355-359; Eales, J., Thorpe, R.S., Malhotra, A., Colonization history and genetic diversity: Adaptive potential in early stage invasions (2010) Molecular Ecology, 19, pp. 2858-2869; Edgar, R.C., MUSCLE: A multiple sequence alignment method with reduced time and space complexity (2004) BMC Bioinformatics, 5, p. 113; Edwards, S.V., Liu, L., Pearl, D.K., High-resolution species trees without concatenation (2007) Proceedings of the National Academy of Sciences USA, 104, pp. 5936-5941; Ersts, P.J., (2014) Geographic Distance Matrix Generator (version 1.2.3), , http://biodiversityinformatics.amnh.org/open_source/gdmg, . [Internet], American Museum of Natural History, Center for Biodiversity and Conservation. Retrieved from, Accessed 5 May 2014; Excoffier, L., Patterns of DNA sequence diversity and genetic structure after a range expansion: Lessons from the infinite–island model (2004) Molecular Ecology, 13, pp. 853-864; Excoffier, L., Lischer, H.E.L., Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows (2010) Molecular Ecology Resources, 10, pp. 564-567; Excoffier, L., Smouse, P., Quattro, J., Analysis of molecular variance inferred from metric distances among DNA haplotypes: Application to human mitochondrial DNA restriction data (1992) Genetics, 131, pp. 479-491; Fairbanks, R.G., A 17,000–year glacio–eustatic sea level record: Influence of glacial melting rates on the Younger Dryas event and deep–ocean circulation (1989) Nature, 342, pp. 637-641; Falk, B.G., Perkins, S.L., Host specificity shapes population structure of pinworm parasites in Caribbean reptiles (2013) Molecular Ecology, 22, pp. 4576-4590; Faubet, P., Waples, R.S., Gaggiotti, O.E., Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates (2007) Molecular Ecology, 16, pp. 1149-1166; Felsenstein, J., (2004) Inferring phylogenies, , Sunderland, Sinauer Associates; Finn, D.S., Bogan, M.T., Lytle, D.A., Demographic stability metrics for conservation prioritization of isolated populations (2009) Conservation Biology, 23, pp. 1185-1194; Gartner, G.E.A., Gamble, T., Jaffe, A., Harrison, A., Losos, J.B., Left–right dewlap asymmetry and phylogeography of Anolis lineatus on Aruba and Curaçao (2013) Biological Journal of the Linnean Society, 110, pp. 409-426; Geneva, A.J., Hilton, J., Noll, S., Glor, R.E., Multilocus phylogenetic analyses of Hispaniolan and Bahamian trunk anoles (distichus species group) (2015) Molecular Phylogenetics and Evolution, 87, pp. 105-117; Glor, R.E., Johnson, M.A., Larson, A., Polymorphic microsatellite loci for the Puerto Rican crested anole (Anolis cristatellus) and their amplification in related Puerto Rican species (2007) Conservation Genetics, 8, pp. 1491-1493; Goldstein, D.B., Pollock, D.D., Launching microsatellites: A review of mutation processes and method for phylogenetic inference (1997) Journal of Heredity, 88, pp. 335-342; Guindon, S., Gascuel, O., A simple, fast and accurate method to estimate large phylogenies by maximum–likelihood (2003) Systematic Biology, 52, pp. 696-704; Gustafson, E.J., Parker, G.R., Relationships between landcover proportion and indices of landscape spatial pattern (1992) Landscape Ecology, 7, pp. 101-110; Hardy, O.J., Charbonnel, N., Fréville, H., Heuertz, M., Microsatellite allele sizes: A simple test to assess their significance on genetic differentiation (2003) Genetics, 163, pp. 1467-1482; Harmon, L.J., Schulte, J.A., II, Larson, A., Losos, J.B., Tempo and mode of evolutionary radiation in iguanian lizards (2003) Science, 301, pp. 961-964; Hearty, P.J., Hollin, J.T., Neumann, A.C., O'Leary, M.J., McCulloch, M., Global sea–level fluctuations during the Last Interglaciation (MIS 5e) (2007) Quaternary Science Reviews, 26, pp. 2090-2112; Heatwole, H., Levins, R., Biogeography of the Puerto Rico Bank: Species–turnover on a small cay, Cayo Ahogado (1973) Ecology, 54, pp. 1042-1055; Heatwole, H., MacKenzie, F., Herpetogeography of Puerto Rico. IV. Paleogeography, faunal similarity an endemism (1967) Evolution, 21, pp. 429-438; Hedrick, P.W., (2009) Genetics of populations, , 4th ed., Sudbury, MA, Jones and Bartlett; Heled, J., Drummond, A.J., Bayesian inference of species trees from multilocus data (2010) Molecular Biology and Evolution, 27, pp. 570-580; Hertz, P.E., Eurythermy and niche breadth in West Indian Anolis lizards: A reappraisal (1983) Advances in herpetology and evolutionary biology, pp. 472-483. , In, A. G. J. Rhodin, #x0026;, K. Miyata, (Eds.),, Cambridge, Museum of Comparative Zoology; Ho, S.Y.W., Phillips, M.J., Cooper, A., Drummond, A.J., Time dependency of molecular rate estimates and systematic overestimation of recent divergence times (2005) Molecular Biology and Evolution, 22, pp. 1561-1568; Huson, D.H., Bryant, D., Application of phylogenetic networks in evolutionary studies (2006) Molecular Biology and Evolution, 23, pp. 254-267; Johnson, K.P., Adler, F.R., Cherry, J.L., Genetic and phylogenetic consequences of island biogeography (2000) Evolution, 52, pp. 387-396; Jombart, T., Adegenet: A R package for the multivariate analysis of genetic markers (2008) Bioinformatics, 24, pp. 1403-1405; Jombart, T., Devillard, S., Balloux, F., Discriminant analysis of principal components: A new method for the analysis genetically structured populations (2010) BMC Genetics, 11, p. 94; Karl, S.A., Toonen, R.J., Grant, W.S., Bowen, B.W., Common misconceptions in molecular ecology: Echoes of the modern synthesis (2012) Molecular Ecology, 21, pp. 4171-4189; Keenan, K., McGinnity, P., Cross, T.R., Crozier, W.W., Prodöhl, P., DiveRsity: An R package for the estimation and exploration of population genetic parameters and their associated errors (2013) Methods in Ecology and Evolution, 4, pp. 782-788; Kolbe, J.J., Glor, R.E., Rodríguez-Schettino, L., Lara, A.C., Larson, A., Losos, J.B., Genetic variation increases during biological invasion by a Cuban lizard (2004) Nature, 431, pp. 177-181; Kolbe, J.J., Larson, A., Losos, J.B., Differential admixture shapes morphological variation among invasive populations of the lizard Anolis sagrei (2007) Molecular Ecology, 16, pp. 1579-1591; Lanfear, R., Welch, J.J., Bromham, L., Watching the clock: Studying rates of molecular evolution between species (2010) Trends in Ecology and Evolution, 25, pp. 495-503; Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Higgins, D.G., Clustal W and Clustal X version 2.0 (2007) Bioinformatics, 23, pp. 947-2948; Librado, P., Rozas, J., DnaSP v5: A software for comprehensive analysis of DNA polymorphism data (2009) Bioinformatics, 25, pp. 1451-1452; Lighty, R.G., Macintyre, I.G., Stuckenrath, R., Acropora palmata reef framework: A reliable indicator of sea level in the Western Atlantic for the past 10,000 years (1982) Coral Reefs, 1, pp. 125-130; Loew, S.S., Williams, D.F., Ralls, K., Pilgrim, K., Fleischer, R.C., Population structure and genetic variation in the endangered giant kangaroo rat (Dipodomys ingens) (2005) Conservation Genetics, 6, pp. 495-510; Losos, J.B., Ricklefs, R.E., Adaptation and diversification on islands (2009) Nature, 457, pp. 830-836; Macey, J.R., Schulte, J.A., II, Ananjeva, N.B., Larson, A., Rastegar-Pouyani, N., Shammakov, S.M., Papenfuss, T.J., Phylogenetic relationships among agamid lizards of the Laudakia caucasia species group: Testing hypotheses of biogeographic fragmentation and an area cladogram for the Iranian Plateau (1998) Molecular Phylogenetics and Evolution, 10, pp. 118-131; Mantel, N.A., The detection of disease clustering and a generalized regression approach (1967) Cancer Research, 27, pp. 209-220; Mayer, G.C., Island lists of West Indian amphibians and reptiles (2012) Bulletin of the Florida Museum of Natural History, 51, pp. 85-166. , . Puerto Rico and the Virgin Islands. In, R. Powell, &, R. W. Henderson, (Eds.); Meiri, S., Oceanic island biogeography: Nomothetic science of the anecdotal (2017) Frontiers of Biogeography, 9 (1); Meirmans, P.G., The trouble with isolation by distance (2012) Molecular Ecology, 21, pp. 2839-2846; Meirmans, P.G., Nonconvergence in Bayesian estimation of migration rates (2014) Molecular Ecology Resources, 14, pp. 726-733; Pannell, J.R., Coalescence in a metapopulation with recurrent local extinction and recolonization (2003) Evolution, 57, pp. 949-961; Papadopoulou, A., Knowles, L.L., Genomic tests of the species-pump hypothesis: Recent island connectivity cycles drive population divergence but not speciation in Caribbean crickets across the Virgin Islands (2015) Evolution, 69, pp. 1501-1517; Peakall, R., Smouse, P.E., Genalex 6: Genetic analysis in Excel. Population genetic software for teaching and research (2006) Molecular Ecology Notes, 6, pp. 288-295; Perry, G., Powell, R., Watson, H., Keeping invasive species off Guana Island, British Virgin Islands (2006) Iguana: Conservation Natural History, and Husbandry of Reptiles, 13, pp. 273-277; Peterson, G.I., Masel, J., Quantitative prediction of molecular clock and Ka/Ks at short timescales (2009) Molecular Biology and Evolution, 26, pp. 2595-2603; (2016) R: A language and environment for statistical computing, , https://www.R-project.org, Vienna, Austria, R Foundation for Statistical Computing, Retrieved from; Rambaut, A., Suchard, M.A., Xie, D., Drummond, A.J., (2013) Tracer v1.5, , http://beast.bio.ed.ac.uk/Tracer, #x0026;, Retrieved from; Raymond, M., Rousset, F., GenePop v1.2: Population genetics software for exact test and ecumenicism (1995) Journal of Heredity, 86, pp. 248-249; Revell, L.J., Harmon, L.J., Langerhans, R.B., Kolbe, J.J., A phylogenetic approach to determining the importance of constraint on phenotypic evolution in the neotropical lizard Anolis cristatellus (2007) Evolutionary Ecology Research, 9, pp. 261-282; Reynolds, R.G., Niemiller, M.L., Hedges, S.B., Dornburg, A., Puente-Rolón, A.R., Revell, L.J., Molecular phylogeny and historical biogeography of West Indian boid snakes (Chilabothrus) (2013) Molecular Phylogenetics and Evolution, 68, pp. 461-470; Rodríguez-Robles, J.A., Jezkova, T., García, M.A., Evolutionary relationships and historical biogeography of Anolis desechensis and Anolis monensis, two lizards endemic to small islands in the eastern Caribbean Sea (2007) Journal of Biogeography, 34, pp. 1546-1558; Rogers, A.R., Harpending, H., Population growth makes waves in the distribution of pairwise genetic differences (1992) Molecular Biology and Evolution, 9, pp. 552-569; Rohling, E.J., Grant, K., Bolshaw, M., Roberts, A.P., Siddall, M., Hemleben, C., Kucera, M., Antarctic temperature and global sea level closely coupled over the past five glacial cycles (2009) Nature Geoscience, 2, pp. 500-504; Rousset, F., Genetic differentiation and estimation of gene flow from F–statistics under isolation by distance (1997) Genetics, 145, pp. 1219-1228; Samarasin, P., Shuter, B.J., Wright, S.I., Rodd, F.H., The problem of estimating recent genetic connectivity in a changing world (2016) Conservation Biology, 31, pp. 126-135; Schuelke, M., An economic method for the fluorescent labelling of PCR fragments (2000) Nature Biotechnology, 18, pp. 233-234; Siddall, M., Rohling, E.J., Almogi-Labin, A., Hemleben, C., Meischner, D., Schmelzer, I., Smeed, D.A., Sea–level fluctuations during the last glacial cycle (2003) Nature, 423, pp. 854-858; Slatkin, M., Gene flow and the geographic structure of natural populations (1987) Science, 236, pp. 787-792; Slatkin, M., Hudson, R.R., Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations (1991) Genetics, 129, pp. 555-562; Stamatakis, A., RaxML–VI–HPC: Maximum likelihood–based phylogenetic analyses with thousands of taxa and mixed models (2006) Bioinformatics, 22, pp. 2688-2690; Stephens, M., Donnelly, P., A comparison of Bayesian methods for haplotype reconstruction from population genotype data (2003) American Journal of Human Genetics, 73, pp. 1162-1169; Stephens, M., Smith, N.J., Donnelly, P., A new statistical method for haplotype reconstruction from population data (2001) American Journal of Human Genetics, 68, pp. 978-989; Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., MEGA6: molecular evolutionary genetics analysis version 6.0 (2013) Molecular Evolutionary Biology, 30, pp. 2725-2729; Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M., Shipley, P., Micro-Checker: Software for identifying and correcting genotyping errors in microsatellite data (2004) Molecular Ecology Notes, 4, pp. 535-538; Vellend, M., Island biogeography of genes and species (2003) The American Naturalist, 162, pp. 358-365; Volkmann, L., Martyn, I., Moulton, V., Spillner, A., Mooers, A.O., Prioritizing populations for conservation using phylogenetic networks (2014) PLoS ONE, 9; Wade, M.J., McCauley, D.E., Extinction and recolonization: Their effects on the genetic differentiation of local populations (1988) Evolution, 42, pp. 995-1005; Whitlock, M.C., McCauley, D.E., Some population genetic consequences of colony formation and extinction: Genetic correlations within founding groups (1990) Evolution, 44, pp. 1717-1724; Whitlock, R., (2004) The consequences of genetic impoverishment for plant community structure and function, , PhD Thesis, University of Sheffield, Sheffield; Williams, E.E., The ecology of colonization as seen in the zoogeography of anoline lizards on small islands (1969) The Quarterly Review of Biology, 44, pp. 345-389; Wilson, G., Rannala, B., Bayesian inference of recent migration rates using multilocus genotypes (2003) Genetics, 163, pp. 1177-1191; Wordley, C., Slate, J., Stapley, J., Mining online genomic resources in Anolis carolinensis facilitates rapid and inexpensive development of cross–species microsatellite markers for the Anolis lizard genus (2011) Molecular Ecology Resources, 11, pp. 126-133; Wright, S., Isolation by distance (1943) Genetics, 28, pp. 114-138; Wright, S., (1977) Evolution and the genetics of populations, volume 3: Experimental results and evolutionary deductions, , Chicago, University of Chicago Press

PY - 2017

Y1 - 2017

N2 - Aim: We examine the influence of fluctuating sea levels in a land-bridge archipelago on the apportioning of intraspecific genetic diversity and divergence in the widespread Puerto Rican crested anole (Anolis cristatellus). We compare three alternative scenarios for genetic diversification in an archipelagic species that contrast the relative influences of periodic isolation versus island connectedness driven by fluctuating sea levels. Our approach combines information from geography and population genetics to assess the influence of island size, island isolation, island historical geography, and population genetic processes such as drift on the contemporary distribution of genetic variation within and among islands. Location: The Puerto Rico Bank in the Caribbean focusing primarily on the Spanish, British and U.S. Virgin Islands. Methods: We used nuclear and mitochondrial DNA sequences and microsatellite genotypes sampled from A. cristatellus populations to investigate: (1) the broad-scale pattern of phylogeographical divergence across Puerto Rico Bank islands and (2) diversification within the Virgin Islands archipelago. For the first component, we used sequence data to reconstruct the relationships among 542 samples from across the species range. For the second component, we examined the relative influences of island size, isolation, and population genetic processes on the distribution of genetic diversity across the Virgin Islands. Results: In the Virgin Islands, A. cristatellus is represented by a monophyletic clade except on the island of Vieques, where two divergent clades coexist. We found evidence for non-equilibrium dynamics in the Virgin Islands, suggesting spatial population expansion during intraglacial periods of low sea level. Main conclusions: We found limited evidence that periods of island isolation affected patterns of genetic diversity and differentiation. Instead, we found that the patterns of genetic diversity and divergence in A. cristatellus in the Virgin Islands archipelago are likely shaped by long-term persistence in the region and periods of population spatial expansion. © 2017 John Wiley & Sons Ltd

AB - Aim: We examine the influence of fluctuating sea levels in a land-bridge archipelago on the apportioning of intraspecific genetic diversity and divergence in the widespread Puerto Rican crested anole (Anolis cristatellus). We compare three alternative scenarios for genetic diversification in an archipelagic species that contrast the relative influences of periodic isolation versus island connectedness driven by fluctuating sea levels. Our approach combines information from geography and population genetics to assess the influence of island size, island isolation, island historical geography, and population genetic processes such as drift on the contemporary distribution of genetic variation within and among islands. Location: The Puerto Rico Bank in the Caribbean focusing primarily on the Spanish, British and U.S. Virgin Islands. Methods: We used nuclear and mitochondrial DNA sequences and microsatellite genotypes sampled from A. cristatellus populations to investigate: (1) the broad-scale pattern of phylogeographical divergence across Puerto Rico Bank islands and (2) diversification within the Virgin Islands archipelago. For the first component, we used sequence data to reconstruct the relationships among 542 samples from across the species range. For the second component, we examined the relative influences of island size, isolation, and population genetic processes on the distribution of genetic diversity across the Virgin Islands. Results: In the Virgin Islands, A. cristatellus is represented by a monophyletic clade except on the island of Vieques, where two divergent clades coexist. We found evidence for non-equilibrium dynamics in the Virgin Islands, suggesting spatial population expansion during intraglacial periods of low sea level. Main conclusions: We found limited evidence that periods of island isolation affected patterns of genetic diversity and differentiation. Instead, we found that the patterns of genetic diversity and divergence in A. cristatellus in the Virgin Islands archipelago are likely shaped by long-term persistence in the region and periods of population spatial expansion. © 2017 John Wiley & Sons Ltd

U2 - 10.1111/jbi.13072

DO - 10.1111/jbi.13072

M3 - Research Article

SN - 0305-0270

VL - 44

SP - 2631

EP - 2647

JO - Journal of Biogeography

JF - Journal of Biogeography

IS - 11

ER -

Archipelagic genetics in a widespread Caribbean anole

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