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Research Article | Open Access

Highly divergent sympatric lineages of Leptotila verreauxi (Aves: Columbidae) suggest a secondary contact area in the Isthmus of Tehuantepec, Mexico

Orlando J. Espinosa-Cháveza,b, Adolfo G. Navarro-Sigüenzaa, Hernando Rodríguez-Correac, Luis A. Sánchez-Gonzáleza()
Museo de Zoología “Alfonso L. Herrera”, Depto. de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México, Apdo. Postal 70-399, CP 04510, Ciudad de México, Mexico
Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio D, 1° Piso, Circuito de Posgrados, Ciudad Universitaria, Universidad Nacional Autónoma de México, Coyoacán, CP 04510, CDMX, Mexico
Escuela Nacional de Estudios Superiores Unidad Morelia, Universidad Nacional Autónoma de México. Antigua Carretera a Pátzcuaro No. 8701 Col. Ex Hacienda de San José de la Huerta, C.P. 58190, Morelia, Michoacán, Mexico
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Abstract

Due to a complex geological and biotic history, the Isthmus of Tehuantepec (IT), has been long recognized as a driver for the evolutionary divergence of numerous lowland and highland taxa. Widely distributed in the lowlands of the American continent, the White-Tipped Dove (Leptotila verreauxi) is a polytypic species with 13 recognized subspecies. Four of these have been recorded in Mexico, and the distribution of three abuts at the IT, suggesting a contact zone. To estimate phylogenetic patterns, divergence times and genetic differentiation, we examined two mtDNA (ND2 and COI) and one nDNA (β-fibint 7) markers. We also used correlative ecological niche models (ENM) to assess whether ecological differences across the IT may have acted as a biogeographical boundary. We estimated paleodistributions during the Middle Holocene, Last Glacial Maximum and Last Interglacial, to evaluate the influence of climate changes on the distribution and demographic changes. Our results showed genetically distinct lineages that diverged approximately 2.5 million years ago. Climatic and ecological factors may have played a dual role in promoting differentiation, but also in the formation of a secondary contact zone in the southern IT. Our ecological niche comparisons indicated that the ecological niche of sympatric lineages at the IT are not identical, suggesting niches divergence; in addition, environmental niche models across the region indicated no abrupt biogeographic barriers, but the presence of regions with low suitability. These results suggest that genetic differentiation originated by a vicariant event probably related to environmental factors, favored the evolution of different ecological niches. Also, the absence of a biogeographic barrier but the presence of less suitable areas in the contact regions, suggest that secondary contact zones may be also maintained by climatic factors for the eastern group, but also by biotic interactions for the western group.

Keywords

Biogeographical boundaryHumid and dry forestsIsthmus of TehuantepecPhylogeographySecondary contact

References

 

Aiello-Lammens, M.E., Boria, R.A., Radosavljevic, A., Vilela, B., Anderson, R.P., 2015. spThin: An R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38, 541-545. https://doi.org/10.1111/ecog.01132.

Crossref Google Scholar
 

Anderson, R.P., Peterson, A.T., Gómez-Laverde, M., 2002. Using niche-based GIS modeling to test geographic predictions of competitive exclusion and competitive release in South American pocket mice. Oikos 98, 3–16.

Crossref Google Scholar
 

Arcangeli, J., Light, J.E., Cervantes, F.A., 2018. Molecular and morphological evidence of the diversification in the gray mouse opossum, Tlacuatzin canescens (Didelphimorphia), with description of a new species. J. Mammal. 99, 138-158. https://doi.org/10.1093/jmammal/gyx173.

Crossref Google Scholar
 

Baehr, J., Fröhlich, K., Botzet, M., Domeisen, D.I.V., Kornblueh, L., Notz, D., et al., 2015. The prediction of surface temperature in the new seasonal prediction system based on the MPI-ESM coupled climate model. Clim. Dyn. 44, 2723-2735. https://doi.org/10.1007/s00382-014-2399–7.

Crossref Google Scholar
 

Bandelt, H-J., Forster, P., Rohl, A., 1999. Median-joining networks for inferring intraspecic phylogenies. Mol. Biol. 16, 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036.

Crossref Google Scholar
 

Barber, B.R., Klicka, J., 2010. Two pulses of diversification across the Isthmus of Tehuantepec in a montane Mexican bird fauna. Proc. R. Soc. A B 277, 2675-2681. https://doi.org/10.1098/rspb.2010.0343.

Crossref Google Scholar
 

Barrier, E., Velasquillo, L., Chavez, M., Gaulon, R., 1998. Neotectonic evolution of the Isthmus of Tehuantepec (southeastern Mexico). Tectonophysics 287, 77-96. https://doi.org/10.1016/S0040-1951(98)80062–0.

Crossref Google Scholar
 

Benham, P.M., Cheviron, Z.A., 2019. Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis). Mol. Ecol. 28, 1765-1783. https://doi.org/10.1111/mec.15049.

Crossref Google Scholar
 

Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J., et al., 2013. GenBank. Nucleic Acids Res. 41, D36-42. https://doi.org/10.1093/nar/gks1195.

Crossref Google Scholar
 
Binford, L.C., 1989. A distributional survey of the birds of the Mexican state of Oaxaca. American Ornithologists’ Union.
Crossref
 

Bradley, R.D., Henson, D.D., Durish, N.D., 2008. Re-evaluation of the geographic distribution and phylogeography of the Sigmodon hispidus complex based on mitochondrial DNA sequences. Southwestern Nat. 53, 301.

Crossref Google Scholar
 

Butler, B.O., Smith, L.L., Flores-Villela, O., 2023. Phylogeography and taxonomy of Coleonyx elegans Gray 1845 (Squamata: Eublepharidae) in Mesoamerica: The Isthmus of Tehuantepec as an environmental barrier. Mol. Phylogenet. Evol. 178, 107632. https://doi.org/10.1016/j.ympev.2022.107632.

Crossref Google Scholar
 

Castillo-Chora, V.D.J., Sánchez-González, L.A., Mastretta-Yanes, A., Prieto-Torres, D.A., Navarro-Sigüenza, A.G., 2021. Insights into the importance of areas of climatic stability in the evolution and maintenance of avian diversity in the Mesoamerican dry forests. Biol. J. Linn. Soc. 132, 741-758. https://doi.org/10.1093/biolinnean/blaa202.

Crossref Google Scholar
 

Cobos, M.E., Townsend Peterson, A., Barve, N., Osorio-Olvera, L., 2019. Kuenm: An R package for detailed development of ecological niche models using Maxent. PeerJ 7, e6281. https://doi.org/10.7717/peerj.6281.

Crossref Google Scholar
 

Dinerstein, E., Olson, D., Joshi, A., Vynne, C., Burgess, N.D., Wikramanayake, E., et al., 2017. An ecoregion-based approach to protecting half the terrestrial realm. BioScience 67, 534-545. https://doi.org/10.1093/biosci/bix014.

Crossref Google Scholar
 
Drummond, A.J., Rambaut, A., 2015. Bayesian evolutionary analysis by sampling trees.In: Bayesian Evolutionary Analysis with BEAST, pp. 79–96.
Crossref
 

Edwards, E.P., Lea, R.B., 1955. Birds of the Monserrate area, Chiapas, Mexico. Condor 57, 31-54. https://doi.org/10.2307/1364696.

Crossref Google Scholar
 

Excoffier, L., Laval, G., Schneider, S., 2005. Arlequin (version 3.0): An integrated software package for population genetics data analysis. Evol. Bioinforma. 1, 47-50. https://doi.org/10.1177/117693430500100003.

Crossref Google Scholar
 
Ferrusquia-Villafranca, I., 1993. Geology of Mexico: a synopsis. Biological Diversity of Mexico: Origins and Distribution.
 
Friedmann, H., Griscom, L., Moore, R.T., 1950. Distributional Check-List of the Birds of Mexico, Part I. Pacific Coast Avifauna Number 29. Cooper Ornithological Club, Berkeley.
 

Fuchs, J., Bowie, R.C.K., Melo, M., Boano, G., Pavia, M., Fjeldsa, J., 2021. Phylogeographical history of the Olive Woodpecker Dendropicos griseocephalus, a species widely distributed across Africa. Ibis 163, 417-428. https://doi.org/10.1111/ibi.12875.

Crossref Google Scholar
 

García-Moreno, J., Navarro-Sigüenza, A.G., Peterson, A.T., Sánchez-González, L.A., 2004. Genetic variation coincides with geographic structure in the common bush-tanager (Chlorospingus ophthalmicus) complex from Mexico. Mol. Phylogenet. Evol. 33, 186-196. https://doi.org/10.1016/j.ympev.2004.05.007.

Crossref Google Scholar
 

Gent, P.R., Danabasoglu, G., Donner, L.J., Holland, M.M., Hunke, E.C., Jayne, S.R., et al., 2011. The community climate system model version 4. J. Clim. 24, 4973-4991. https://doi.org/10.1175/2011JCLI4083.1.

Crossref Google Scholar
 
Gill, F., Donsker, D., Rasmussen, P., 2021. IOC World Bird List, 13.1. https://doi.org/10.14344/IOC.ML.13.1.
Crossref
 

Glor, R.E., Warren, D., 2011. Testing ecological explanations for biogeographic boundaries. Evolution 65, 673-683. https://doi.org/10.1111/j.1558-5646.2010.01177.x.

Crossref Google Scholar
 

Gray, L.N., Barley, A.J., Poe, S., Thomson, R.C., Nieto-Montes de Oca, A., Wang, I.J., 2019. Phylogeography of a widespread lizard complex reflects patterns of both geographic and ecological isolation. Mol. Ecol. 28, 644-657. https://doi.org/10.1111/mec.14970.

Crossref Google Scholar
 

Hafner, M.S., Sudman, P.D., Villablanca, F.X., Spradling, T.A., Demastes, J.W., Nadler, S.A., 1994. Disparate rates of molecular evolution in cospeciating hosts and parasites. Science 265, 1087-1090. https://doi.org/10.1126/science.8066445.

Crossref Google Scholar
 
Hartl, D.L., Clark, A.G., 1997. Principles of population genetics. Sinauer associates Sunderland.
 

Hasumi, H., Emori, S., 2004. K-1 Coupled GCM (MIROC) Description. K-1 Tech. Rep. 1 34.

Google Scholar
 

Hebert, P.D.N., Stoeckle, M.Y., Zemlak, T.S., Francis, C.M., 2004. Identification of birds through DNA barcodes. PLoS Biol. 2, e312. https://doi.org/10.1371/journal.pbio.0020312.

Crossref Google Scholar
 

Hijmans, R.J., Cameron, S.E., Parra, J.L., Jones, P.G., Jarvis, A., 2005. Very high-resolution interpolated climate surfaces for global land areas. Int. J. Climatol. 25, 1965-1978. https://doi.org/10.1002/joc.1276.

Crossref Google Scholar
 
Hogan, K.M., 1999. White-tipped dove (Leptotila verreauxi). In: Poole, A., Gill, F. (Eds.), The Birds of North America, No. 436. The Birds of North America, Inc., Philadelphia, P A.
Crossref
 

Hogner, S., Laskemoen, T., Lifjeld, J.T., Porkert, J., Kleven, O., Albayrak, T., et al., 2012. Deep sympatric mitochondrial divergence without reproductive isolation in the common redstart Phoenicurus phoenicurus. Ecol. Evol. 2, 2974-2988. https://doi.org/10.1002/ece3.398.

Crossref Google Scholar
 

Howell, S.N.G., Webb, S., 1995. A Guide to the Birds of Mexico and Northern Central America. Oxford University Press, Oxford.

Crossref
 

Huelsenbeck, J.P., Ronquist, F., 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754-755. https://doi.org/10.1093/bioinformatics/17.8.754.

Crossref Google Scholar
 

Johnson, K.P., Clayton, D.H., 2000. Nuclear and mitochondrial genes contain similar phylogenetic signal for pigeons and doves (Aves: Columbiformes). Mol. Phylogenet. Evol. 14, 141-151. https://doi.org/10.1006/mpev.1999.0682.

Crossref Google Scholar
 

Johnson, K.P., Weckstein, J.D., 2011. The Central American land bridge as an engine of diversification in New World doves. J. Biogeogr. 38, 1069-1076. https://doi.org/10.1111/j.1365-2699.2011.02501.x.

Crossref Google Scholar
 

Katoh, K., Standley, D.M., 2013. MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Mol. Biol. Evol. 30, 772-780. https://doi.org/10.1093/molbev/mst010.

Crossref Google Scholar
 

Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., et al., 2012. Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647-1649. https://doi.org/10.1093/bioinformatics/bts199.

Crossref Google Scholar
 

Lanfear, R., Frandsen, P.B., Wright, A.M., Senfeld, T., Calcott, B., 2017. Partitionfinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Mol. Biol. Evol. 34, 772-773. https://doi.org/10.1093/molbev/msw260.

Crossref Google Scholar
 

Llanes-Quevedo, A., Mastretta-Yanes, A., Sánchez-González, L.A., Castillo-Chora, V.J., Navarro-Sigüenza, A.G., 2022. The tangled evolutionary history of a long-debated Mesoamerican taxon: The Velazquez Woodpecker (Melanerpes santacruzi, Aves: Picidae). Mol. Phylogenet. Evol. 170, 107445. https://doi.org/10.1016/j.ympev.2022.107445.

Crossref Google Scholar
 

Lorenz, T.C., 2012. Polymerase chain reaction: Basic protocol plus troubleshooting and optimization strategies. J. Vis. Exp. 63, e3998. https://doi.org/10.3791/3998.

Crossref Google Scholar
 

Machado-Stredel, F., Cobos, M.E., Peterson, A.T., 2021. A simulation-based method for selecting calibration areas for ecological niche models and species distribution models. Front. Biogeogr. 13, e48814. https://doi.org/10.21425/f5fbg48814.

Crossref Google Scholar
 

McCloy, C., Ingle, J.C., Barron, J.A., 1988. Neogene stratigraphy, foraminifera, diatoms, and depositional history of Maria Madre Island, Mexico: Evidence of early Neogene marine conditions in the southern Gulf of California. Mar. Micropaleontol. 13, 193-212. https://doi.org/10.1016/0377-8398(88)90003–5.

Crossref Google Scholar
 

Morrone, J.J., 2010. Fundamental biogeographic patterns across the Mexican Transition Zone: an evolutionary approach. Ecography 33, 355-361. https://doi.org/10.1111/j.1600-0587.2010.06266.x.

Crossref Google Scholar
 

Morrone, J.J., 2014. Biogeographical regionalisation of the Neotropical region. Zootaxa 3782, 1-110. https://doi.org/10.11646/zootaxa.3782.1.1.

Crossref Google Scholar
 

Mulcahy, D.G., Morrill, B.H., Mendelson III, J.R., 2006. Historical biogeography of lowland species of toads (Bufo) across the Trans-Mexican Neovolcanic Belt and the Isthmus of Tehuantepec. J. Biogeogr. 33, 1889–1904.

Crossref Google Scholar
 

Navarro-Sigüenza, A.G., Townsend Peterson, A., Nyari, A., García-Deras, G.M., García-Moreno, J., 2008. Phylogeography of the Buarremon brush-finch complex (Aves, Emberizidae) in Mesoamerica. Mol. Phylogenet. Evol. 47, 21-35. https://doi.org/10.1016/j.ympev.2007.11.030.

Crossref Google Scholar
 

Navarro-Sigüenza, A.G., Rebon-Gallardo, M.F., Gordillo-Martinez, A., Peterson, A.T., Berlanga-García, H., Sánchez-González, L.A., 2014. Biodiversidad de aves en Mexico. Rev. Mex. Biodivers. 85, 476-495. https://doi.org/10.7550/rmb.41882.

Crossref Google Scholar
 

Nei, M., 1987. Molecular Evolutionary Genetics. Columbia University Press, New York.

Crossref
 

Omland, K.E., Baker, J.M., Peters, J.L., 2006. Genetic signatures of intermediate divergence: population history of Old and New World Holarctic ravens (Corvus corax). Mol. Ecol. 15, 795-808. https://doi.org/10.1111/j.1365-294X.2005.02827.x.

Crossref Google Scholar
 

Ornelas, J.F., Sosa, V., Soltis, D.E., Daza, J.M., González, C., Soltis, P.S., et al., 2013. Comparative phylogeographic analyses illustrate the complex evolutionary history of threatened cloud forests of northern Mesoamerica. PLoS One 8, 56283. https://doi.org/10.1371/journal.pone.0056283.

Crossref Google Scholar
 

Ortiz-Ramírez, M.F., Andersen, M.J., Zaldívar-Riverón, A., Ornelas, J.F., Navarro-Sigüenza, A.G., 2016. Geographic isolation drives divergence of uncorrelated genetic and song variation in the Ruddy-capped Nightingale-Thrush (Catharus frantzii; Aves: Turdidae). Mol. Phylogenet. Evol. 94, 74-86. https://doi.org/10.1016/j.ympev.2015.08.017.

Crossref Google Scholar
 

Ortiz-Ramírez, M.F., Sánchez-González, L.A., Castellanos-Morales, G., Ornelas, J.F., Navarro-Sigüenza, A.G., 2018. Concerted Pleistocene dispersal and genetic differentiation in passerine birds from the Tres Marias Archipelago, Mexico. Auk 135, 716-732. https://doi.org/10.1642/auk-17-190.1.

Crossref Google Scholar
 

Osorio-Olvera, L., Lira-Noriega, A., Soberón, J., Peterson, A.T., Falconi, M., Contreras-Díaz, R.G., et al., 2020. ntbox: An r package with graphical user interface for modelling and evaluating multidimensional ecological niches. Methods Ecol. Evol. 11, 1199-1206. https://doi.org/10.1111/2041-210X.13452.

Crossref Google Scholar
 

Pereira, S.L., Johnson, K.P., Clayton, D.H., Baker, A.J., 2007. Mitochondrial and nuclear DNA sequences support a Cretaceous origin of Columbiformes and a dispersal-driven radiation in the Paleogene. Syst. Biol. 56, 656-672. https://doi.org/10.1080/10635150701549672.

Crossref Google Scholar
 

Peterson, A.T., Soberón, J., Sánchez-Cordero, V., 1999. Conservatism of ecological niches in evolutionary time. Science 285, 1265-1267. https://doi.org/10.1126/science.285.5431.1265.

Crossref Google Scholar
 

Phillips, S.J., Anderson, R.P., Dudik, M., Schapire, R.E., Blair, M.E., 2017. Opening the black box: an open-source release of Maxent. Ecography 40, 887-893. https://doi.org/10.1111/ecog.03049.

Crossref Google Scholar
 

Pons, J-M., Masson, C., Olioso, G., Fuchs, J., 2019. Gene flow and genetic admixture across a secondary contact zone between two divergent lineages of the Eurasian Green Woodpecker Picus viridis. J. Ornithol. 160, 935-945. https://doi.org/10.1007/s10336-019-01675–6.

Crossref Google Scholar
 

Prychitko, T.M., Moore, W.S., 1997. The utility of DNA sequences of an intron from the β-Fibrinogen gene in phylogenetic analysis of woodpeckers (Aves: Picidae). Mol. Phylogenet. Evol. 8, 193-204. https://doi.org/10.1006/mpev.1997.0420.

Crossref Google Scholar
 

Pybus, O.G., 2006. Model selection and the molecular clock. PLoS Biol. 4, 686-688. https://doi.org/10.1371/journal.pbio.0040151.

Crossref Google Scholar
 
QGIS Development Team, 2022. QGIS Geographic Information System.
 
Rambaut, A., 2009. FigTree v1.4.3. http://tree.bio.ed.ac.uk/software/figtree/, 4.22.23.
 

Rambaut, A., Drummond, A.J., Xie, D., Baele, G., Suchard, M.A., 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Syst. Biol. 67, 901-904. https://doi.org/10.1093/sysbio/syy032.

Crossref Google Scholar
 

Ramírez-Díaz, C.J., Ramírez-Morillo, I.M., Cortés-Flores, J., de-Nova, J.A., Duno de Stefano, R., Fernández-Concha, G.C., 2023. Biogeographical History of the Yucatan Peninsula Endemic Flora (Spermatophyta) from a Phylogenetic Perspective. Harvard Pap. Bot. 28, 99-120, https://doi.org/10.3100/hpib.v28iss1.2023.n13.

Crossref Google Scholar
 

Ramos-Onsins, S.E., Rozas, J., 2002. Statistical properties of new neutrality tests against population growth. Mol. Biol. Evol. 19, 2092-2100. https://doi.org/10.1093/oxfordjournals.molbev.a004034.

Crossref Google Scholar
 

Rodríguez-Correa, H., González-Rodríguez, A., Oyama, K., 2017. Perspectivas de la ecologia molecular en un pais megadiverso. Rev. Mex. Biodivers. 88, 3-13. https://doi.org/10.1016/j.rmb.2017.10.002.

Crossref Google Scholar
 

Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574. https://doi.org/10.1093/bioinformatics/btg180.

Crossref Google Scholar
 

Rozas, J., Ferrer-Mata, A., Sánchez-Del Barrio, J.C., Guirao-Rico, S., Librado, P., Ramos-Onsins, S.E., et al., 2017. DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol. Biol. Evol. 34, 3299-3302. https://doi.org/10.1093/molbev/msx248.

Crossref Google Scholar
 
Sambrook, J., Russell, D.W., 2006. Purification of Nucleic Acids by Extraction with Phenol: chloroform. CSH Protoc. https://doi.org/10.1101/pdb.prot4455, 2006, pdb.prot4455.
Crossref
 

Sánchez-González, L.A., Castillo-Chora, V.J., Arbeláez-Cortés, E., Navarro-Sigüenza, A.G., 2021. Diversification and secondary contact in the magpie-jays (Calocitta) throughout the pacific lowlands of Mesoamerica. J. Zool. Syst. Evol. Res. 59, 2371-2386. https://doi.org/10.1111/jzs.12571.

Crossref Google Scholar
 

Sánchez-González, L.A., Cayetano, H., Prieto-Torres, D.A., Rojas-Soto, O.R., Navarro-Sigüenza, A.G., 2023. The role of ecological and geographical drivers of lineage diversification in the Squirrel cuckoo Piaya cayana in Mexico: a mitochondrial DNA perspective. J. Ornithol. 164, 37-53. https://doi.org/10.1007/S10336-022-02008-W.

Crossref Google Scholar
 

Sangster, G., Sweet, A.D., Johnson, K.P., 2018. Paraclaravis, a new genus for the Purple-winged and Maroon-chested Ground-doves (Aves: Columbidae). Zootaxa 4461, 134. https://doi.org/10.11646/zootaxa.4461.1.10.

Crossref Google Scholar
 

Seutin, G., Ratcliffe, L.M., Boag, P.T., 1995. Mitochondrial DNA homogeneity in the phenotypically diverse redpoll finch complex (Aves: Carduelinae: Carduelis flammea-hornemanni). Evolution 49, 962-973. https://doi.org/10.2307/2410418.

Crossref Google Scholar
 

Shackleton, N.J., 2000. The 100,000-year Ice-age cycle identified and found to lag temperature, carbon dioxide, and orbital eccentricity. Science 289, 1897–1902.

Crossref Google Scholar
 

Silvestro, D., Michalak, I., 2012. RaxmlGUI: A graphical front-end for RAxML. Org. Divers. Evol. 12, 335-337. https://doi.org/10.1007/s13127-011-0056–0.

Crossref Google Scholar
 

Smith, A.B., Godsoe, W., Rodríguez-Sánchez, F., Wang, H.H., Warren, D., 2019. Niche estimation above and below the species level. Trends Ecol. Evol. 34, 260-273. https://doi.org/10.1016/j.tree.2018.10.012.

Crossref Google Scholar
 

Sorenson, M.D., Ast, J.C., Dimcheff, D.E., Yuri, T., Mindell, D.P., 1999. Primers for a PCR-based approach to mitochondrial genome sequencing in birds and other vertebrates. Mol. Phylogenet. Evol. 12, 105-114. https://doi.org/10.1006/mpev.1998.0602.

Crossref Google Scholar
 

Sosa-López, J.R., González, C., Navarro-Sigüenza, A.G., 2013. Vocal geographic variation in Mesoamerican Common Bush Tanagers (Chlorospingus ophthalmicus). Wilson J. Ornithol. 125, 24-33. https://doi.org/10.1676/12-051.1.

Crossref Google Scholar
 

Stamatakis, A., Hoover, P., Rougemont, J., 2008. A rapid bootstrap algorithm for the RAxML Web Servers. Syst. Biol. 57, 758-771. https://doi.org/10.1080/10635150802429642.

Crossref Google Scholar
 

Steel, M., McKenzie, A., 2001. Properties of phylogenetic trees generated by Yule-type speciation models. Math. Biosci. 170, 91-112. https://doi.org/10.1016/S0025-5564(00)00061–4.

Crossref Google Scholar
 

Stull, G.W., 2023. Evolutionary origins of the eastern North American-Mesoamerican floristic disjunction: Current status and future prospects. Am. J. Bot. 110, e16142. https://doi.org/10.1002/ajb2.16142.

Crossref Google Scholar
 

Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J., Rambaut, A., 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evol. 4. https://doi.org/10.1093/ve/vey016.

Crossref Google Scholar
 

Sweet, A.D., Johnson, K.P., 2015. Patterns of diversification in small New World ground doves are consistent with major geologic events. Auk 132, 300-312. https://doi.org/10.1642/auk-14-193.1.

Crossref Google Scholar
 

Sweet, A.D., Maddox, J.D., Johnson, K.P., 2017. A complete molecular phylogeny of Claravis confirms its paraphyly within small New World ground-doves (Aves: Peristerinae) and implies multiple plumage state transitions. J. Avian Biol. 48, 459-464. https://doi.org/10.1111/jav.01077.

Crossref Google Scholar
 

Tominaga, K., Watanabe, K., Kakioka, R., Mori, S., Jeon, S.R., 2009. Two highly divergent mitochondrial DNA lineages within Pseudogobio esocinus populations in central Honshu, Japan. Ichthyol. Res. 56, 195-199. https://doi.org/10.1007/s10228-008-0071–0.

Crossref Google Scholar
 

Tsai, W.L.E., Mota-Vargas, C., Rojas-Soto, O., Bhowmik, R., Liang, E.Y., Maley, J.M., et al., 2019. Museum genomics reveals the speciation history of Dendrortyx wood-partridges in the Mesoamerican highlands. Mol. Phylogenet. Evol. 136, 29-34. https://doi.org/10.1016/j.ympev.2019.03.017.

Crossref Google Scholar
 

Vázquez-Miranda, H., Navarro-Sigüenza, A.G., Omland, K.E., 2009. Phylogeography of the Rufous-naped Wren (Campylorhynchus rufinucha): speciation and hybridization in Mesoamerica. Auk 126, 765-778. https://doi.org/10.1525/auk.2009.07048.

Crossref Google Scholar
 

Warren, D.L., Matzke, N.J., Cardillo, M., Baumgartner, J.B., Beaumont, L.J., Turelli, M., et al., 2021. ENMTools 1.0: an R package for comparative ecological biogeography. Ecography 44, 504-511. https://doi.org/10.1111/ecog.05485.

Crossref Google Scholar
 
Wei, T., Simko, V., 2021. R Package “Corrplot”: Visualization of a Correlation Matrix.
 

Whitmore, F.C., Stewart, R.H., 1965. Miocene mammals and Central American seaways. Science 148, 180-185. https://doi.org/10.1126/science.148.3667.180.

Crossref Google Scholar
 

Wogau, K.H., Arz, H.W., Bohnel, H.N., Nowaczyk, N.R., Park, J., 2019. High resolution paleoclimate and paleoenvironmental reconstruction in the northern Mesoamerican frontier for prehistory to historical times. Quat. Sci. Rev. 226, 106001. https://doi.org/10.1016/j.quascirev.2019.106001.

Crossref Google Scholar
 

Wyatt Durham, J., Arellano, A.R.V., Peck JR. J.H., 1955. Evidence for no Cenozoic Isthmus of Tehuantepec seaways. GSA Bull. 66, 977-992. https://doi.org/10.1130/0016-7606(1955)66[977:EFNCIO]2.0.CO;2.

Crossref Google Scholar
 

Xiao, J.H., Wang, N.X., Murphy, R.W., Cook, J., Jia, L.Y., Huang, D.W., 2012. Wolbachia infection and dramatic intraspecific mitochondrial DNA divergence in a fig wasp. Evolution 66, 1907-1916. https://doi.org/10.1111/j.1558-5646.2011.01561.x.

Crossref Google Scholar
 

Zarza, E., Reynoso, V.H., Emerson, B.C., 2008. Diversification in the northern neotropics: mitochondrial and nuclear DNA phylogeography of the iguana Ctenosaura pectinata and related species. Mol. Ecol. 17, 3259-3275. https://doi.org/10.1111/j.1365-294X.2008.03826.x.

Crossref Google Scholar
Avian Research
Volume 15 Issue 1,
March 2024
Article number: 100160
DOI: 10.1016/j.avrs.2024.100160
Cite this article:
Espinosa-Chávez OJ, Navarro-Sigüenza AG, Rodríguez-Correa H, et al. Highly divergent sympatric lineages of Leptotila verreauxi (Aves: Columbidae) suggest a secondary contact area in the Isthmus of Tehuantepec, Mexico. Avian Research, 2024, 15(1): 100160. https://doi.org/10.1016/j.avrs.2024.100160
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