Abstract
The Pleistocene climate cycles and mountain uplift both affected the diversification of taxa in Mesoamerica. Yet, phylogeographic breaks and demographic responses of co-distributed taxa are not congruent. Investigation of more species with widespread distributions across Mexico and Central America will help shed light on how Earth historical events shaped biodiversity in this region. The Azure-crowned Hummingbird (Amazilia cyanocephala) is widely distributed from eastern Mexico into Central America and has been divided into three subspecies by morphology and geographic isolation. To investigate the evolutionary history of the species, we sequenced a non-coding mtDNA fragment along with a nuclear marker across its distribution, and analysed morphological and ecological variation and distributional projections derived from ecological niche modelling. Overall, mtDNA supported genetic differentiation among A. cyanocephala populations, which generally supports the existence of four lineages: two A. c. cyanocephala lineages separated by the Isthmus of Tehuantepec (east and west), A. c. guatemalensis populations separated by the Motagua-Polochic-Jocotán fault system, and the isolated A. c. chlorostephana in Honduras and Nicaragua. However, morphological data were not consistent with this phylogeographic result. The potential distribution of suitable habitat for A. cyanocephala was expanded during the Last Glacial Maximum and more contracted and fragmented during the Last Inter-Glacial and the Present. These models are consistent with a preglacial demographic expansion in A. c. cyanocephala. Mitochondrial genetic diversity and current precipitation seasonality were negatively correlated when analysing all populations. We suggest that isolation and habitat differences have both played a role in the recent diversification of A. cyanocephala. Inferences about the demographic consequences of isolation and subspecies recognition await further study.
Zusammenfassung
Phylogeographie, Morphologie und ökologische Nischenmodellierung zur Erforschung der Evolutionsgeschichte der Blaukopfamazilie ( Amazilia cyanocephala Trochilidae)
Sowohl die Klimazyklen des Pleistozäns als auch die Hebung der Gebirge beeinflussten die Diversifizierung der Taxa in Mesoamerika. Dennoch sind die phylogeographischen Brüche und die demographischen Reaktionen von sich parallel verbreitenden Taxa nicht kongruent. Eine Untersuchung von mehr Arten mit großflächiger Verbreitung in Mexico und Zentralamerika wird bei der Aufklärung helfen, wie erdgeschichtliche Prozesse die Biodiversität in diesen Regionen geformt haben mögen. Die Blaukopfamazilie (Amazilia cyanocephala) ist von Ost-Mexico bis nach Zentralamerika weit verbreitet und wird entsprechend ihrer Morphologie und geographischen Isolierung in drei Unterarten eingeteilt. Zur Untersuchung der Evolutionsgeschichte dieser Arten sequenzierten wir ein nicht-kodierendes mtDNA-Fragment zusammen mit einem Marker über die ganze Verbreitung hinweg und analysierten die morphologischen und ökologischen Unterschiede sowie die Verbreitungsvorhersagen aus Modellen für ökologische Nischen. Insgesamt unterstützte die mtDNA die genetische Differenzierung zwischen den A. cyanocephala-Populationen, die wiederum generell das Vorhandensein von vier Linien unterstützt: zwei A. c. cyanocephala-Linien, die durch den Isthmus von Tehuantepec in Ost und West getrennt sind, eine A. c. guatemalensis-Population, getrennt durch die Motagua-Polochic-Jocotán-Verwerfung und die isolierte A. c. chlorostephana-Population in Honduras und Nicaragua. Die morphologischen Daten stimmten jedoch nicht mit den phylogeographischen überein. Die Verbreitung potentiell geeigneter Habitate für A. cyanocephala vergrößerte sich während des Letzteiszeitlichen Maximums und schrumpfte wieder und fragmentierte sich während des letzten Interglazials und der Gegenwart. Diese Modelle passen zu einer voreiszeitlichen Ausbreitung von A. c. cyanocephala. Mitochondriale genetische Vielfalt und die aktuelle Niederschlagssaisonalität waren in der Analyse bei allen Populationen negativ korreliert. Wir nehmen an, dass sowohl die Isolation als auch Habitatunterschiede bei der jüngsten Diversifizierung von A. cyanocephala eine Rolle gespielt haben. Schlussfolgerungen zu den demographischen Folgen der Isolation und der Anerkennung von Unterarten sind von weiteren Untersuchungen abhängig.
Similar content being viewed by others
Data availability
All unique sequences used in this study have been deposited in Genbank under accession numbers: 20454 locus: MT674641–MT674667, CR: MT674632–MT674640. The full data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa, and the true skill statistic (TSS). J Appl Ecol 43:1223–1232
Alvarado-Sizzo H, Casas A, Parra F, Arreola-Nava HJ, Terrazas T, Sánchez C (2018) Species delimitation in the Stenocereus griseus (Cactaceae) species complex reveals a new species, S huastecorum. PLoS ONE 13:e0190385
Alvarez S, Salter JF, McCormack JE, Milá B (2016) Speciation in mountain refugia: phylogeography and demographic history of the pine siskin and black-capped siskin complex. J Avian Biol 47:335–345
American Ornithologist’s Union (AOU) (1998) Check-list of North American Birds, 7th edn. Washington, DC
Andermann T, Fernandes AM, Olsson U, Töpel M, Pfeil B, Oxelman B, Aleixo A, Faircloth BC, Antonelli A (2019) Allele phasing greatly improves the phylogenetic utility of ultraconserved elements. Syst Biol 68:32–46
Anderson DL, Wiedenfeld DA, Bechard MJ, Novak SJ (2004) Avian diversity in the Moskitia region of Honduras. Ornith Neotrop 15:447–482
Arbeláez-Cortés E, Navarro-Sigüenza AG (2013) Molecular evidence of the taxonomic status of western Mexican populations of Phaethornis longirostris (Aves: Trochilidae). Zootaxa 3716:81–97
Backström N, Fagerberg S, Ellegren H (2008) Genomics of natural bird populations: a gene-based set of reference markers evenly spread across the avian genome. Mol Ecol 17:964–980
Barber BR, Klicka J (2010) Two pulses of diversification across the Isthmus of Tehuantepec in a montane Mexican bird fauna. Proc R Soc Lond B 277:2675–2681
Barve N, Barve V, Jiménez-Valverde A, Lira-Noriega A, Maher SP, Peterson AT, Soberón J, Villalobos F (2011) The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol Modell 222:1810–1819
Bonaccorso E, Navarro-Sigüenza AG, Sánchez-González LA, Peterson AT, García-Moreno J (2008) Genetic differentiation of the Chlorospingus ophthalmicus complex in Mexico and Central America. J Avian Biol 39:311–321
Booth TH, Nix HA, Busby JR, Hutchinson MF (2014) BIOCLIM: the first species distribution modelling package, its early applications and relevance to most current MAXENT studies. Divers Distribut 20:1–9
Bouckaert R, Heled J, Kühnert D, Vaughan T, Wu C, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput Biol 10:e1003537
Braconnot P, Otto-Bliesner B, Harrison S, Joussaume S, Peterschmitt JY, Abe-Ouchi A, Crucifix M, Driesschaert E, Fichefet T, Hewitt CD, Kageyama M (2007) Results of PMIP2 coupled simulations of the mid-holocene and last glacial maximum-part 2: feedbacks with emphasis on the location of the ITCZ and mid- and high latitudes heat budget. Clim Past 3:279–296
Broennimann O, Fitzpatrick MC, Pearman PB, Petitpierre B, Pel-lissier L, Yoccoz NG, Thuiller W, Fortin MJ, Randin C, Zim-mermann NE, Graham CH, Guisan A (2012) Measuring ecological niche overlap from occurrence and spatial environ- mental data. Glob Ecol Biogeogr 21:481–497
Castoe TA, Daza JM, Smith EN, Sasa MM, Kuch U, Campbell JA, Chippindale PT, Parkinson CL (2009) Comparative phylogeography of pitvipers suggests a consensus of ancient Middle American highland biogeography. J Biogeogr 36:88–103
Chaves JA, Pollinger JP, Smith TB, LeBuhn G (2007) The role of geography and ecology in shaping the phylogeography of the speckled hummingbird (Adelomyia melanogenys) in Ecuador. Mol Phylogenet Evol 43:795–807
Chesser RT, Billerman SM, Burns KJ, Cicero C, Dunn JL, Kratter AW, Lovette IJ, Mason NA, Rasmussen PC, Remsen Jr JV, Stotz DF, Winker K (2020) Sixty-first Supplement to the American Ornithological Society’s Check-list of North American Birds. Auk 137:ukaa030
Clarke KR, Warwick RM (2001) Changes in marine communities: an approach to statistical analysis and interpretation, 2nd edn. PRIMER-E Ltd, Plymouth
Clement M, Snell Q, Walker P, Posada D, Crandall K (2002) TCS: estimating gene genealogies. Parallel Distrib Process Symp Inter Proc 2:184
Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129
Cortés-Rodríguez N, Hernández-Baños BE, Navarro-Sigüenza AG, Peterson AT, García-Moreno J (2008) Phylogeography and population genetics of the Amethyst-throated Hummingbird (Lampornis amethystinus). Mol Phylogenet Evol 48:1–11
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9:772
Daza JM, Castoe TA, Parkinson CL (2010) Using regional comparative phylogeographic data from snake lineages to infer historical processes in Middle America. Ecography 33:343–354
del Hoyo J, Elliott A, Sargatal J (1999) Handbook of the birds of the world, Barn-owls to hummingbirds, vol 5. Lynx Editions, Barcelona
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Mol Biol Evol 22:1185–1192
Drummond AJ, Bouckaert RR (2015) Bayesian evolutionary analysis with BEAST 2. Cambridge University Press, Cambridge
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform 1:47–50
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49
Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
Gill F, Donsker D, Rasmussen P (eds) (2020) IOC World List (v10.2). https://doi.org/10.14344/IOC.ML.10.2
González C, Ornelas JF, Gutiérrez-Rodríguez C (2011) Selection and geographic isolation influence hummingbird speciation: genetic, acoustic and morphological divergence in the wedge-tailed sabrewing (Campylopterus curvipennis). BMC Evol Biol 11:38
Gotlieb Y, García Girón JD (2020) The role of land use conversion in shaping the land cover of the Central American Dry Corridor. Land Use Policy 94:104351
Graham A (1999) Studies in Neotropical paleobotany. XIII. An Oligo-Miocene palynoflora from Simojovel (Chiapas, Mexico). Amer J Bot 86:17–31
Griscom L (1932) The distribution of bird-life in Guatemala. Bull Am Mus Nat Hist 64:1–458
Gutiérrez-García TA, Vázquez-Domínguez E (2013) Consensus between genes and stones in the biogeographic and evolutionary history of Central America. Quat Res 79:311–324
Gutiérrez-Rodríguez C, Ornelas JF, Rodríguez-Gómez F (2011) Chloroplast DNA phylogeography of a distylous shrub (Palicourea padifolia, Rubiaceae) reveals past fragmentation and demographic expansion in Mexican cloud forests. Mol Phylogenet Evol 61:603–615
Heller R, Chikhi L, Siegismund HR (2013) The confounding effect of population structure on Bayesian skyline plot inferences of demographic history. PLoS ONE 8:e62992
Hernández-Soto M, Licona-Vera Y, Lara C, Ornelas JF (2018) Molecular and climate data reveal expansion and genetic differentiation of Mexican Violet-ear Colibri thalassinus thalassinus (Aves: Trochilidae) populations separated by the Isthmus of Tehuantepec. J Ornithol 159:687–702
Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978
Howell TR (1965) New subspecies of birds from the lowland pine savanna of northeastern Nicaragua. Auk 82:438–464
Howell SNG, Webb S (1995) A guide to the birds of Mexico and northern Central America. Oxford University Press, New York
Jiménez RA, Ornelas JF (2016) Historical and current introgression in a Mesoamerican hummingbird species complex: a biogeographic perspective. PeerJ 4:e1556
Johnsgard PA (1997) The Hummingbirds of North America. Smithsonian Institution Press, Washington, D.C.
Kruskal JB (1964) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29:115–129
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
Leigh JW, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116
Licona-Vera Y, Ornelas JF (2014) Genetic, ecological and morphological divergence between populations of the endangered Mexican Sheartail Hummingbird (Doricha eliza). PLoS ONE 9:e101870
Licona-Vera Y, Ornelas JF, Wethington S, Bryan KB (2018) Pleistocene range expansions promote divergence with gene flow between migratory and sedentary populations of Calothorax hummingbirds. Biol J Linn Soc 124:645–667
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789
Maldonado-Sánchez D, Gutiérrez-Rodríguez C, Ornelas JF (2016) Genetic divergence in the common bush-tanager Chlorospingus ophthalmicus (Aves: Emberizidae) throughout Mexican cloud forests: the role of geography, ecology and Pleistocene climatic fluctuations. Mol Phylogenet Evol 99:76–88
Malpica A, Ornelas JF (2014) Postglacial northward expansion and genetic differentiation between migratory and sedentary populations of the broad-tailed hummingbird (Selasphorus platycercus). Mol Ecol 23:435–452
McGuire JA, Witt CC, Remsen JV Jr, Corl A, Rabosky DL, Altshuler DL, Dudley R (2014) Molecular phylogenetics and the diversification of hummingbirds. Curr Biol 24:910–916
Milá B, Smith TB, Wayne RK (2007) Speciation and rapid phenotypic differentiation in the yellow-rumped warbler Dendroica coronata complex. Mol Ecol 16:159–173
Miller MJ, Lelevier MJ, Bermingham E, Klicka JT, Escalante P, Winker K (2011) Phylogeography of the Rufous-tailed Hummingbird (Amazilia tzacatl). Condor 113:806–816
Moonlight PW, Richardson JE, Tebbitt MC, Thomas DC, Hollands R, Peng CI, Hughes M (2015) Continental-scale diversification patterns in a megadiverse genus: the biogeography of neotropical Begonia. J Biogeogr 42:1137–1149
Morrone JJ (2014) Biogeographical regionalisation of the neotropical region. Zootaxa 3782:1–21
Müller J, Müller K, Neinhuis C, Quandt D (2010) Phylogenetic data editor. PhyDE-1 v0:9971
Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858
Nei M, Li WH (1979) Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc Natl Acad Sci USA 76:5269–5273
Nigenda-Morales SF, Gompper ME, Valenzuela-Galván D, Lay AR, Kapheim KM, Hass C, Booth-Binczik SD, Binczik GA, Hirsch BT, McColgin M, Koprowski JL (2019) Phylogeographic and diversification patterns of the white-nosed coati (Nasua narica): evidence for south-to-north colonization of North America. Mol Phylogenet Evol 131:149–163
Oksanen J (2006–2011) Multivariate analysis of ecological communities in R: vegan tutorial. http://cc.oulu.fi/~jarioksa/popular.html.
Orme CDL, Davies RG, Burgess M, Eigenbrod F, Pickup N, Olson VA, Webster AJ, Ding T-S, Rasmussen PC, Ridgely RS, Stattersfield AJ, Bennett PM, Blackburn TM, Gaston KJ, Owens IPF (2020) Global hotspots of species richness are not congruent with endemism or threat. Nature 436:1016–1019
Ornelas JF (2010) Nests, eggs, and young of the Azure-crowned Hummingbird (Amazilia cyanocephala). Wilson J Ornithol 122:592–597
Ornelas JF, González C (2014) Interglacial genetic diversification of Moussonia deppeana (Gesneriaceae), a hummingbird-pollinated, cloud forest shrub in northern Mesoamerica. Mol Ecol 23:4119–4136
Ornelas JF, Sosa V, Soltis DE, Daza JM, González C, Soltis PS, Gutiérrez-Rodríguez C, Espinosa de los Monteros A, Castoe TA, Bell C, Ruiz-Sanchez E, (2013) Comparative phylogeographic analyses illustrate the complex evolutionary history of threatened cloud forests of northern Mesoamerica. PLoS ONE 8:e56283
Ornelas JF, González C, Espinosa de los Monteros A, Rodríguez-Gómez F, García-Feria LM (2014) In and out of Mesoamerica: temporal divergence of Amazilia hummingbirds pre-dates the orthodox account of the completion of the Isthmus of Panama. J Biogeogr 41:168–181
Ornelas JF, González C, Hernández-Baños BE, García-Moreno J (2016) Molecular and iridescent feather reflectance data reveal recent genetic diversification and phenotypic differentiation in a cloud forest hummingbird. Ecol Evol 6:1104–1127
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Pulgarín-R PC, Burg TM (2012) Genetic signals of demographic expansion in Downy Woodpecker (Picoides pubescens) after the Last North American Glacial Maximum. PLoS ONE 7:e40412
Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904
Ramírez-Barahona S, Eguiarte LE (2013) The role of glacial cycles in promoting genetic diversity in the Neotropics: the case of cloud forests during the last glacial maximum. Ecol Evol 3:725–738
Rocha-Méndez A, Sánchez-González LA, González C, Navarro-Sigüenza AG (2019) The geography of evolutionary divergence in the highly endemic avifauna from the Sierra Madre del Sur. Mex BMC Evol Biol 19:237
Rodríguez-Gómez F, Ornelas JF (2014) Genetic divergence of the Mesoamerican azure-crowned hummingbird (Amazilia cyanocephala, Trochilidae) across the Motagua-Polochic-Jocotán fault system. J Zool Syst Evol Res 52:142–153
Rodríguez-Gómez F, Ornelas JF (2015) At the passing gate: past introgression in the process of species formation between Amazilia violiceps and A. viridifrons hummingbirds along the Mexican Transition Zone. J Biogeogr 42:1305–1318
Rodríguez-Gómez F, Ornelas JF (2018) Genetic structuring and secondary contact in the white-chested Amazilia hummingbird species complex. J Avian Biol 49:e01536
Rodríguez-Gómez F, Gutiérrez-Rodríguez C, Ornelas JF (2013) Genetic, phenotypic and ecological divergence with gene flow at the Isthmus of Tehuantepec: the case of the azure-crowned hummingbird (Amazilia cyanocephala). J Biogeogr 40:1360–1373
Rogers AR (1995) Genetic evidence for a Pleistocene population explosion. Evolution 49:608–615
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise differences. Mol Biol Evol 9:552–569
Rovito SM, Wake DB, Papenfuss TJ, Parra-Olea G, Muñoz-Alonso A, Vásquez-Almazán CR (2012) Species formation and geographical range evolution in a genus of Central American cloud forest salamanders (Dendrotriton). J Biogeogr 39:1251–1265
Rozas J, Ferrer-Mata A, Sánchez-DelBarrio JC, Guirao-Rico S, Librado P, Ramos-Onsins SE, Sánchez-Gracia A (2017) DnaSP 6: DNA sequence polymorphism analysis of large data sets. Mol Biol Evol 34:3299–3302
Russell RW, Carpenter FL, Hixon MA, Paton DC (1994) The impact of variation in stopover habitat quality on migrant rufous hummingbirds. Conserv Biol 8:483–490
Schneider S, Excoffier L (1999) Estimation of demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152:1079–1089
Smith BT, Escalante P, Hernández-Baños BE, Navarro-Sigüenza AG, Rohwer S, Klicka J (2011) The role of historical and contemporary processes on phylogeographic structure and genetic diversity in the Northern Cardinal, Cardinalis cardinalis. BMC Evol Biol 11:136
Soberón J, Peterson AT (2005) Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodivers Info 2:1–10
Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Steven JP, Miroslav D, Schapire RE (2017) Maxent software for modeling species niches and distributions (version 3.4.1). http://biodiversityinformatics.amnh.org/open_source/maxent/. Accessed on 5 Dec 2019 (Internet)
Stiles FG, Remsen JV Jr, McGuire JA (2017) The generic classification of the Trochilini (Aves: Trochilidae): reconciling taxonomy with phylogeny. Zootaxa 4353:401–424
Still CJ, Foster PN, Schneider SH (1999) Simulating the effects of climate change on tropical montane cloud forests. Nature 398:608–610
Strubbe D, Beauchard O, Matthysen E (2015) Niche conservatism among nonnative vertebrates in Europe and North America. Ecography 38:321–329
Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526
Tovilla-Sierra RD, Herrera-Alsina LH, Bribiesca R, Arita HT (2019) The spatial analysis of biological interactions: morphological variation responding to the co-occurrence of competitors and resources. J Avian Biol 50:e02223
Tsai WL, Mota-Vargas C, Rojas-Soto O, Bhowmik R, Liang EY, Maley JM, Zarza E, McCormack JE (2019) Museum genomics reveals the speciation history of Dendrortyx wood-partridges in the Mesoamerican highlands. Mol Phylogenet Evol 136:29–34
Tsai WL, Schedl ME, Maley JM, McCormack JE (2020) More than skin and bones: comparing extraction methods and alternative sources of DNA from avian museum specimens. Mol Ecol Resour 20:1220–1227
Venkatraman MX, Deraad DA, Tsai WL, Zarza E, Zellmer AJ, Maley JM, McCormack JE (2019) Cloudy with a chance of speciation: integrative taxonomy reveals extraordinary divergence within a Mesoamerican cloud forest bird. Biol J Linn Soc 126:1–15
Warren DL, Glor REG, Turelli M (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62:2868–2883
Zamudio-Beltrán LE, Hernández-Baños BE (2015) A multilocus analysis provides evidence formore than one species within Eugenes fulgens (Aves: Trochilidae). Mol Phylogenet Evol 90:80–84
Zamudio-Beltrán LE, Hernández-Baños BE (2018) Genetic and morphometric divergence in the Garnet-Throated Hummingbird Lamprolaima rhami (Aves: Trochilidae). PeerJ 6:e5733
Zamudio-Beltrán LE, Ornelas JF, Malpica A, Hernández-Baños BE (2020a) Genetic and morphological differentiation among populations of the Rivoli’s Hummingbird (Eugenes fulgens) species complex (Aves: Trochilidae). Auk 137:ukaa032
Zamudio-Beltrán LE, Licona-Vera Y, Hernández-Baños BE, Klicka J, Ornelas JF (2020b) Phylogeography of the widespread white-eared hummingbird (Hylocharis leucotis): preglacial expansion and genetic differentiation of populations separated by the Isthmus of Tehuantepec. Biol J Linn Soc 130:247–267
Acknowledgements
We thank the Moore Laboratory of Zoology at Occidental College for access to specimens and tissue sampling. Whitney Tsai helped in the lab with data collection and Ernesto A. López-Huicochea with data analysis. We also thank John McCormack, Carina Carneiro de Melo Moura and three anonymous reviewers for their valuable criticisms and suggestions. We obtained collecting permits to conduct this work from the Secretaría de Medio Ambiente y Recursos Naturales, Instituto Nacional de Ecología, Dirección General de Vida Silvestre (permit numbers: INE, SEMARNAT, SGPA/DGVS/02038/07, 01568/08, 02517/09) and the Guatemalan Government through the Universidad San Carlos de Guatemala collecting permits granted to R. A. Jiménez (permit numbers: 1-005-2010, 14815). FRG was supported by a postdoctoral scholarship (237125) from the CONACyT Becas al Extranjero program.
Funding
Financial support was provided by grants 25922-N and 61710 (awarded to JFO) from the Consejo Nacional de Ciencia y Tecnología (CONACyT) and UDG-PTC-1476 (awarded to FRG) from the Incorporación de Nuevos Profesores de Tiempo Completo program (Secretaría de Educación Pública).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by M. Wink.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Rodríguez-Gómez, F., Licona-Vera, Y., Silva-Cárdenas, L. et al. Phylogeography, morphology and ecological niche modelling to explore the evolutionary history of Azure-crowned Hummingbird (Amazilia cyanocephala, Trochilidae) in Mesoamerica. J Ornithol 162, 529–547 (2021). https://doi.org/10.1007/s10336-020-01853-x
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10336-020-01853-x