Abstract
Historical geological events and climatic changes have played important roles in shaping population differentiation and distribution within species. In this study, we analysed the distribution, expansion and colonization patterns, and genetic differentiation among Psittacanthus rhynchanthus populations in Mesoamerica. Specifically, we determine the effects of major historical events and geographic barriers on population divergence using nuclear and chloroplast DNA sequence data and the impact of Pleistocene glacial cycles on the distribution dynamics of P. rhynchanthus using ecological niche modelling (ENM). Our results showed that P. rhynchanthus populations split into two lineages, one distributed on the Yucatán Peninsula and the second along the Pacific and Atlantic slopes and Honduras, approximately 1 million years ago. The two lineages were fragmented at the last interglacial according to ENM predictions and experienced postglacial range expansion during the Last Glacial Maximum. Analysis of climate differentiation and niche models showed that both lineages have different climatic preferences, where the climatic characteristics of the Yucatán populations are not fully represented in the rest of the distribution range of P. rhynchanthus. Additionally, our study suggests that Pleistocene expansion of suitable habitat, environmental segregation (ecological barrier between regions) and, perhaps host shifts, have acted as the isolation mechanisms between the two lineages. Our results provide new insight as to understanding the distribution and phylogeographic patterns and the possible mechanisms underlying intraspecific evolutionary relationships of plants in the Mesoamerican tropical lowlands.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
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. https://doi.org/10.1111/j.1365-2664.2006.01214.x
Anselmetti F, Ariztegui D, Hodell DA, Hillesheim MB, Brenner M, Gilli A, McKenzie JA, Mueller AD (2006) Late Quaternary climate-induced lake level variations in Lake Petén Itzá, Guatemala, inferred from seismic stratigraphic analysis. Palaeogeogr Palaeoclim Palaeoecol 230:52–69. https://doi.org/10.1016/j.palaeo.2005.06.037
Arteaga MC, McCormack JE, Eguiarte LE, Medellín RA (2011) Genetic admixture in multidimensional environmental space: asymmetrical niche similarity promotes gene flow in armadillos (Dasypus novemcinctus). Evolution 65:2470–2480. https://doi.org/10.1111/j.1558-5646.2011.01329.x
Baena-Díaz F, Ramírez-Barahona S, Ornelas JF (2018) Hybridization and differential introgression associated with environmental shifts in a mistletoe species complex. Sci Rep 8:5591. https://doi.org/10.1038/s41598-018-23707-6
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 Model 222:1810–1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011
Becerra JX (2005) Timing the origin and expansion of the Mexican tropical dry forest. Proc Natl Acad Sci USA 102:10919–10923. https://doi.org/10.1073/pnas.0409127102
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. Diversity Distrib 20:1–9. https://doi.org/10.1111/ddi.12144
Braconnot P, Otto-Bliesner B, Harrison S, Joussaume S, Peterchmitt JY, Abe-Ouchi A, Crucifix M, Driesschaert E, Fichefet Th, Hewitt CD, Kageyama M, Kitoh A, Loutre M-F, Marti O, Merkel U, Ramstein G, Valdes P, Weber L, Yu Y, Zhao Y (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. https://doi.org/10.5194/cp-3-279-2007
Bush MB, Correa-Metrio AY, Hodell DA, Brenner M, Anselmetti FS, Ariztegui D, Mueller AD, Curtis JH, Grzesik DA, Burton C, Gilli A (2009) Re-evaluation of climate change in lowland Central America during the last glacial maximum using new sediment cores from Lake Petén- Itzá, Guatemala. In: Vimeuz F, Sylvestre F, Khodri M (eds) Past climate variability in South America and Surrounding Regions, from the Last Glacial Maximum to the Holocene, vol. 14. Springer, Houten, pp 113–128
Caballero M, Lozano-García S, Vázquez-Selem L, Ortega B (2010) Evidencias de cambio climático y ambiental en registros glaciales y en cuencas lacustres del centro de México durante el último máximo glacial. Bol Soc Geol Mex 62:359–377
Caballero-Rodríguez D, Correa-Metrio A, Lozano-García S, Sosa-Nájera S, Ortega B, Sanchez-Dzib Y, Aguirre-Navarro K, Sandoval-Montaño A (2018) Late-Quaternary spatiotemporal dynamics of vegetation in Central Mexico. Rev Palaeobot Palynol 250:44–52. https://doi.org/10.1016/j.revpalbo.2017.12.004
Carnaval AC, Moritz C (2008) Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest. J Biogeogr 35:1187–1201. https://doi.org/10.1111/j.1365-2699.2007.01870.x
Carnaval AC, Hickerson MJ, Haddad CFB, Rodrigues MT, Moritz C (2009) Stability predicts genetic diversity in the Brazilian Atlantic Forest hotspot. Science 23:785–789. https://doi.org/10.1126/science.1166955
Carvalho YGS, Vitorino LC, de Souza UJB, Bessa LA (2019) Recent trends in research on the genetic diversity of plants: implications for conservation. Diversity 11:62. https://doi.org/10.3390/d11040062
Cavender-Bares J, Gonzalez-Rodriguez A, Pahlich A, Koehler K, Deacon N (2011) Phylogeography and climatic niche evolution in live oaks (Quercus series Virentes) from the tropics to the temperate zone. J Biogeogr 38:962–981. https://doi.org/10.1111/j.1365-2699.2010.02451.x
Cavers S, Navarro C, Lowe AJ (2003) Chloroplast DNA phylogeography reveals colonization history of a Neotropical tree, Cedrela odorata L., in Mesoamerica. Molec Ecol 12:1451–1460. https://doi.org/10.1046/j.1365-294X.2003.01810.x
Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547. https://doi.org/10.1890/11-1952.1
Chávez-Pesqueira M, Núñez-Farfán J (2016) Genetic diversity and structure of wild populations of Carica papaya in Northern Mesoamerica inferred by nuclear microsatellites and chloroplast markers. Ann Bot (Oxford) 118:1293–1306. https://doi.org/10.1093/aob/mcw183
Chiang TY, Schaal BA, Peng CI (1998) Universal primers for amplification and sequencing a noncoding spacer between the atpB and rbcL genes of chloroplast DNA. Bot Bull Acad Sinica 39:245–250
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Molec Ecol 9:1657–1659. https://doi.org/10.1046/j.1365-294x.2000.01020.x
Colin R, Eguiarte LE (2016) Phylogeographic analyses and genetic structure illustrate the complex evolutionary history of Phragmites australis in Mexico. Amer J Bot 103:876–887. https://doi.org/10.3732/ajb.1500399
Colinvaux PA, de Oliveira PE, Moreno JE, Miller MC, Bush MB (1996) A long pollen record from lowland Amazonia: forest and cooling in glacial times. Science 274:85–87. https://doi.org/10.1126/science.274.5284.85
Colinvaux PA, Irion G, Rasanen ME, Bush MB, de Mello J (2001) A paradigm to be discarded: geological and paleoecological data falsify the Haffer & Prance refuge hypothesis of Amazonian speciation. Amazoniana 16:609–646
Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9 and earlier. User’s Guide and application. Available at: http://purl.oclc.org/estimates. Accessed 23 Aug 2019
Corander J, Sirén J, Arjas E (2008) Bayesian spatial modeling of genetic population structure. Comput Stat 23:111–129. https://doi.org/10.1007/s00180-007-0072-x
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Meth 9:772. https://doi.org/10.1038/nmeth.2109
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. https://doi.org/10.1111/j.1600-0587.2010.06281.x
De-Nova A, Medina R, Montero JC, Weeks A, Rosell JA, Olson ME, Eguiarte LE, Magallón S (2012) Insights into the historical construction of species-rich Mesoamerican seasonally dry tropical forests: the diversification of Bursera (Burseraceae, Sapindales). New Phytol 193:276–287. https://doi.org/10.1111/j.1469-8137.2011.03909.x
Díaz Infante S, Lara C, Arizmendi MC, Eguiarte LE, Ornelas JF (2016) Reproductive ecology and isolation of Psittacanthus calyculatus and P. auriculatus mistletoes (Loranthaceae). PeerJ 4:e2491. https://doi.org/10.7717/peerj.2491
Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure from small quantities of fresh leaf tissue. Phytochem Bull 19:11–15
Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214. https://doi.org/10.1186/1471-2148-7-214
Drummond AJ, Rambaut A, Shapiro B, Pybus OG (2005) Bayesian coalescent inference of past population dynamics from molecular sequences. Molec Biol Evol 22:1185–1192. https://doi.org/10.1093/molbev/msi103
Dupanloup I, Schneider S, Excoffier L (2002) A simulated annealing approach to define the genetic structure of populations. Molec Ecol 11:2571–2581. https://doi.org/10.1046/j.1365-294X.2002.01650.x
Elith J, Phillips SJ, Hastie T, Dudík M, Chee YE, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Diversity Distrib 17:43–57. https://doi.org/10.1111/j.1472-4642.2010.00725.x
Excoffier L, Smouse P, Quattro J (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50
Falk DA, Holsinger KE (1991) Genetics and conservation of rare plants. Oxford University Press, New York
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environm Conservation 24:38–49
Fu YX (1997) Statistical neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925
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. https://doi.org/10.1186/1471-2148-11-38
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. https://doi.org/10.1046/j.1461-0248.2001.00230.x
Guevara-Chumacero LM, López-Wilchis R, Pedroche FF, Juste J, Ibáñez C, Barriga-Sosa IDLA (2010) Molecular phylogeography of Pteronotus davyi (Chiroptera: Mormoopidae) in Mexico. J Mammol 91:220–232. https://doi.org/10.1644/08-MAMM-A-212R3.1
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. Molec Phylogen Evol 61:603–615. https://doi.org/10.1016/j.ympev.2011.08.023
Haffer J (1969) Speciation in Amazonian forest birds. Science 165:131–136. https://doi.org/10.1126/science.165.3889.131
Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl Acids Symp Ser 41:95–98. https://doi.org/10.12691/ajidm-4-3-3
Harpending RC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Human Biol 66:591–600
Heled J, Drummond AJ (2010) Bayesian inference of species trees from multilocus data. Molec Biol Evol 27:570–580. https://doi.org/10.1093/molbev/msp274
Hewitt GM (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276. https://doi.org/10.1111/j.1095-8312.1996.tb01434.x
Hewitt GM (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. https://doi.org/10.1038/35016000
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. https://doi.org/10.1002/joc.1276
Hodell DA, Anselmetti FS, Ariztegui D, Brenner M, Curtis JH, Gilli A, Grzesik DA, Guilderson TJ, Müller AD, Bush MB, Correa-Metrio A, Escobar J, Kutterolf S (2008) An 85-ka record of climate change in lowland Central America. Quatern Sci Rev 27:1152–1165. https://doi.org/10.1016/j.quascirev.2008.02.008
Hsieh TC, Ma KH, Chao A (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Meth Ecol Evol 7:1451–1456. https://doi.org/10.1111/2041-210X.12613
Jaramillo-Correa JP, Beaulieu J, Khasa DP, Bousquet J (2009) Inferring the past from the present phylogeographic structure of North American forest trees: seeing the forest for the genes. Canad J Pl Res 39:286–307. https://doi.org/10.1139/X08-181
Knowles LL (2008) Why does a method that fails continue to be used? Evolution 62:2713–2717. https://doi.org/10.1111/j.1558-5646.2008.00481.x
Kuijt J (1987) Novelties in Mesoamerican mistletoes (Loranthaceae and Viscaceae). Ann Missouri Bot Gard 74:511–532
Kuijt J (2009) Monograph of Psittacanthus (Loranthaceae). Syst Bot Monogr 86:1–362
Landis JR, Koch GG (1977) The measurement of observer agreement for categorical data. Biometrics 33:159–174
Lavin M, Mathews S, Hughes C (1991) Chloroplast DNA variation in Gliricidia sepium (Leguminosae): intraspecific phylogeny and tokogeny. Amer J Bot 78:1576–1585. https://doi.org/10.1002/j.1537-2197.1991.tb11437.x
León-Camargo D, Rangel-Ch JO (2015) Interacción colibrí-flor en tres remanentes de bosque tropical seco (BST) del Municipio de Chimichagua (Cesar Colombia). Caldasia 37:107–123
Leyden BW (1984) Guatemalan forest synthesis after Pleistocene aridity. Proc Natl Acad Sci USA 81:4856–4859. https://doi.org/10.1073/pnas.81.15.4856
Licona-Vera Y, Ortiz-Rodriguez AE, Vásquez-Aguilar AA, Ornelas JF (2018) Lay mistletoes on the Yucatan Peninsula: post-glacial expansion and genetic differentiation of Psittacanthus mayanus (Loranthaceae). Bot J Linn Soc 186:334–360. https://doi.org/10.1093/botlinnean/box098
Lira-Noriega A, Toro-Núñez O, Oaks JR, Mort ME (2015) The roles of history and ecology in chloroplast phylogeographic patterns of the bird-dispersed plant parasite Phoradendron californicum (Viscaceae) in the Sonoran Desert. Amer J Bot 102:149–164. https://doi.org/10.3732/ajb.1400277
Liu C, White M, Newell G (2013) Selecting thresholds for the prediction of species occurrence with presence-only data. J Biogeogr 40:778–789. https://doi.org/10.1111/jbi.12058
Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annual Rev Ecol Syst 15:65–95. https://doi.org/10.1146/annurev.es.15.110184.000433
Luna-Vega I (2008) Aplicaciones de la biogeografía histórica a la distribución de las plantas mexicanas. Revista Mex Biodivers 79:217–241
Manolopoulou I, Emerson BC (2012) Phylogeographic ancestral inference using the coalescent model on haplotype trees. J Comp Biol 19:745–755. https://doi.org/10.1089/cmb.2012.0038
Manolopoulou I, Legarreta L, Emerson BC, Brooks S, Tavaré S (2011) A Bayesian approach to phylogeographic clustering. Interface Focus 1:909–921. https://doi.org/10.1098/rsfs.2011.0054
Manolopoulou I, Hille A, Emerson B (2020) BPEC: an R package for Bayesian phylogeographic and ecological clustering. J Stats Softw (accepted). arXiv:1604.01617
Masson-Delmotte V, Kageyama M, Braconnot P, Charbit S, Krinner G, Ritz C, Guilyardi E, Jouzel J, Abe-Ouchi A, Crucifix M, Gladstone RM, Hewitt CD, Kitoh A, LeGrande AN, Marti O, Merkel U, Motoi T, Ohgaito R, Otto-Bliesner B, Peltier WR, Ross I, Valdes PJ, Vettoretti G, Weber SL, Wolk F, Yu Y (2006) Past and future polar amplification of climate change: climate model intercomparisons and ice-core constraints. Clim Dynam 26:513–529. https://doi.org/10.1007/s00382-005-0081-9
Mastretta-Yanes A, Moreno-Letelier A, Piñero D, Jorgensen TH, Emerson BC (2015) Biodiversity in the Mexican highlands and the interaction of geology, geography and climate within the Trans- Mexican Volcanic Belt. J Biogeogr 42:1586–1600. https://doi.org/10.1111/jbi.12546
Mastretta-Yanes A, Xue AT, Moreno-Letelier A, Jorgensen TH, Alvarez N, Piñero D, Emerson BC (2018) Long-term in situ persistence of biodiversity in tropical sky islands revealed by landscape genomics. Molec Ecol 27:432–448. https://doi.org/10.1111/mec.14461
McCormack JE, Heled J, Delaney KS, Peterson AT, Knowles LL (2011) Calibrating divergence times on species trees versus gene trees: implications for speciation history of Aphelocoma jays. Evolution 65:184–202. https://doi.org/10.1111/j.1558-5646.2010.01097.x
Montaño-Arias G, Luna-Vega I, Morrone JJ, Espinosa D (2018) Biogeographical identity of the Mesoamerican dominion wwith emphasis on seasonally dry tropical forests. Phytotaxa 376:277–290. https://doi.org/10.11646/phytotaxa.376.6.3
Moreno-Letelier A, Piñero D (2009) Phylogeographic structure of Pinus strobiformis Engelm. across the Chihuahuan Desert filter-barrier. J Biogeogr 36:121–131. https://doi.org/10.1111/j.1365-2699.2008.02001.x
Morrone JJ (2005) Hacia una síntesis biogeográfica de México. Revista Mex Biodivers 76:207–252
Morrone JJ (2014) Biogeographical regionalisation of the Neotropical region. Zootaxa 3782:1–110. https://doi.org/10.11646/zootaxa.3782.1.1
Mueller AD, Anselmetii FS, Ariztequi D, Brenner M, Hodell DA, Curtis JH, Escobar J, Gilli A, Grzesik DA, Guilderson TP, Kutterolf S, Plötze (2010) Late Quaternary palaeoenvironment of northern Guatemala: evidence from deep drill cores and seismic statigraphy of Lake Petén Itzá. Sedimentology 57:1220–1245. https://doi.org/10.1111/j.1365-3091.2009.01144.x
Ornelas JF, González C (2014) Interglacial genetic diversification of Moussonia deppeana (Gesneriaceae), a hummingbird-pollinated, cloud forest shrub in northern Mesoamerica. Molec Ecol 23:4119–4136. https://doi.org/10.1111/mec.12841
Ornelas JF, Rodríguez-Gómez F (2015) Influence of Pleistocene glacial/interglacial cycles of the genetic structure of the mistletoe cactus Rhipsalis baccifera (Cactaceae) in Mesoamerica. J Heredity 106:196–210. https://doi.org/10.1093/jhered/esu113
Ornelas JF, Ruiz-Sanchez E, Sosa V (2010) Phylogeography of Podocarpus matudae (Podocarpaceae): pre-Quaternary relicts in northern Mesoamerican cloud forests. J Biogeogr 37:2384–2396. https://doi.org/10.1111/j.1365-2699.2010.02372.x
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. https://doi.org/10.1371/journal.pone.0056283
Ornelas JF, Gándara E, Vásquez-Aguilar AA, Ramírez-Barahona S, Ortiz-Rodriguez AE, González C, Mejía Saules MT, Ruiz-Sanchez E (2016) A mistletoe tale: postglacial invasion of Psittacanthus schiedeanus (Loranthaceae) to Mesoamerican cloud forests revealed by molecular data and species distribution modeling. BMC Evol Biol 16:78. https://doi.org/10.1186/s12862-016-0648-6
Ornelas JF, Licona-Vera Y, Vásquez-Aguilar AA (2018a) Genetic differentiation and fragmentation in response to climate change of the narrow endemic Psittacanthus auriculatus. Trop Conservation Sci 11:1–15. https://doi.org/10.1177/1940082918755513
Ornelas JF, Licona-Vera Y, Ortiz-Rodriguez AE (2018b) Contrasting responses of generalized/specialized mistletoe-host interactions under climate change. Écoscience 25:223–234. https://doi.org/10.1080/11956860.2018.1439297
Ornelas JF, Ortiz-Rodriguez AE, Ruiz-Sanchez E, Sosa V, Pérez-Farrera MA (2019a) Ups and downs: genetic differentiation among populations of the Podocarpus (Podocarpaceae) species in Mesoamerica. Molec Phylogen Evol 138:17–30. https://doi.org/10.1016/j.ympev.2019.05.025
Ornelas JF, García JM, Ortiz-Rodriguez AE, Licona-Vera Y, Gándara E, Molina-Freaner F, Vásquez-Aguilar AA (2019b) Tracking host trees: phylogeography of endemic Psittacanthus sonorae (Loranthaceae) mistletoe in the Sonoran Desert. J Heredity 110:229–246. https://doi.org/10.1093/jhered/esy065
Ortiz-Rodriguez A, Ornelas JF, Ruiz-Sanchez E (2018a) A jungle tale: molecular phylogeny and divergence time estimates of the Desmopsis-Stenanona clade (Annonaceae) in Mesoamerica. Molec Phylogen Evol 122:80–94. https://doi.org/10.1016/j.ympev.2018.01.021
Ortiz-Rodriguez AE, Guerrero EY, Ornelas JF (2018b) Phylogenetic position of Neotropical Bursera-specialist mistletoes: the evolution of deciduousness and succulent leaves in Psittacanthus (Loranthaceae). Bot Sci 96:443–461. https://doi.org/10.17129/botsci.1961
Otto-Bliesner BL, Marshall SJ, Overpeck JT, Miller GH, Hu A (2006) Simulating Arctic climate warmth and icefield retreat in the Last Interglaciation. Science 311:1751–1753. https://doi.org/10.1126/science.1120808
Otto-Bliesner BL, Hewitt CD, Marchitto TM, Brady E, Abe-Ouchi A, Crucifix M, Murakami S, Weber SL (2007) Last Glacial Maximum ocean thermohaline circulation: PMIP2 model intercomparisons and data constraints. Geophys Res Lett 34:L12706. https://doi.org/10.1029/2007GL029475
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Pennington RT, Lavin M, Prado DE, Pendry CA, Pell SK, Butterworth CA (2004) Historical climate change and speciation: neotropical seasonally dry forest plants show patterns of both Tertiary and Quaternary diversification. Phil Trans R Soc Lond B 359:515–537. https://doi.org/10.1098/rstb.2003.1435
Pérez-Crespo MJ, Ornelas JF, González-Rodríguez A, Ruiz-Sanchez E, Vásquez-Aguilar AA, Ramírez-Barahona S (2017) Phylogeography and population differentiation in the Psittacanthus calyculatus (Loranthaceae) mistletoe: a complex scenario of climate-volcanism interaction along the Trans-Mexican Volcanic Belt. J Biogeogr 44:2501–2514. https://doi.org/10.1111/jbi.13070
Petit RJ, Duminil J, Fineschi S, Hampe A, Salvini D, Vendramin GG (2005) Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations. Molec Ecol 14:689–701. https://doi.org/10.1111/j.1365-294X.2004.02410.x
Pfenninger M, Posada D (2002) Phylogeographic history of the land snail Candidula unifasciata (Helicellinae, Stylommatophora): fragmentation, corridor migration, and secondary contact. Evolution 56:1776–1788. https://doi.org/10.1111/j.0014-3820.2002.tb00191.x
Phillips SJ, Anderson RP, Schapire RE (2006) Maximum entropy modeling of species geographic distributions. Ecol Model 190:231–259. https://doi.org/10.1016/j.ecolmodel.2005.03.026
Pons O, Petit RJ (1996) Measuring and testing genetic differentiation with ordered versus unordered alleles. Genetics 144:1237–1245
Prance GT (1973) Phytogeographic support for the theory of Pleistocene forest refuges in the Amazon Basin, based upon evidence from distribution pattern in Caryocaraceae, Chrysobalanaceae, Dichapetalaceae and Lecythidaceae. Acta Amazon 3:5–28
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. https://doi.org/10.1002/ece3.483
Ramírez-Barahona S, Eguiarte LE (2014) Changes in the distribution of cloud forests during the last glacial period predict the patterns of genetic diversity and demographic history of the tree fern Alsophila firma (Cyatheaceae). J Biogeogr 41:2396–2407. https://doi.org/10.1111/jbi.12396
Ramírez-Barahona S, González C, González-Rodríguez A, Ornelas JF (2017) The influence of climatic niche preferences on the population genetic structure of a mistletoe species complex. New Phytol 214:1751–1761. https://doi.org/10.1111/nph.14471
Ramos-Onsins R, Rozas R (2002) Statistical properties of new neutrality tests against population growth. Molec Biol Evol 19:2092–2100
Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise differences. Molec Biol Evol 9:552–569. https://doi.org/10.1093/oxfordjournals.molbev.a040727
Rosell JA, Olson ME, Weeks A, De-Nova JA, Medina Lemos R, Pérez Camacho J, Feria TP, Gómez-Bermejo R, Montero JC, Eguiarte LE (2010) Diversification in species complexes: tests of species origin and delimitation in the Bursera simaruba clade of tropical trees (Burseraceae). Molec Phylogen Evol 57:798–811. https://doi.org/10.1016/j.ympev.2010.08.004
Ruiz-Sanchez E, Ornelas JF (2014) Phylogeography of Liquidambar styraciflua (Altingiaceae) in Mesoamerica: survivors of a Neogene widespread temperate forest (or cloud forest) in North America? Ecol Evol 4:311–328. https://doi.org/10.1002/ece3.938
Ruiz-Sanchez E, Specht CD (2014) Ecological speciation in Nolina parviflora (Asparagaceae): lacking spatial connectivity along of the Trans-Mexican Volcanic Belt. PLoS ONE 9:e98754. https://doi.org/10.1371/journal.pone.0098754
Rzedowski J (1963) El extremo boreal del bosque tropical siempre verde en Norteamérica continental. Vegetation 11:173–198. https://doi.org/10.1007/BF00298831
Sánchez-González LA, Navarro-Sigüenza AG, Ornelas JF, Morrone JJ (2013) What’s in a name? Mesoamerica. Revista Mex Biodivers 84:1305–1308. https://doi.org/10.7550/rmb.34171
Savage JM (1966) The origins and history of the Central American herpetofauna. Copeia 1966:719–766
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 AB, Godsoe W, Rodríguez-Sánchez F, Wang HH, Warren D (2019) Niche estimation above and below the species level. Trends Ecol Evol 34:261–273. https://doi.org/10.1016/j.tree.2018.10.012
Suárez-Atilano M, Burbrink F, Vázquez-Domínguez E (2014) Phylogeographical structure within Boa constrictor imperator across the lowlands and mountains of Central America and Mexico. J Biogeogr 41:2371–2384. https://doi.org/10.1111/jbi.12372
Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293. https://doi.org/10.1126/science.3287615
Taberlet P, Gielly L, Pautou G, Bouvet J (1991) Universal primers for amplification of three non-coding regions of chloroplast DNA. Pl Molec Biol 17:1105–1109. https://doi.org/10.1007/BF00037152
Tajima F (1989) Statistical-method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Vargas-Rodríguez YL, Platt WJ, Urbatsch LE, Foltz DW (2015) Large scale patterns of genetic variation and differentiation in sugar maple from tropical Central America to temperate North America. BMC Evol Biol 15:257. https://doi.org/10.1186/s12862-015-0518-7
Willis CG, Franzone BF, Zhenxiang X, Davis CC (2014) The establishment of Central American migratory corridors and the biogeographic origins of seasonally dry tropical forests in Mexico. Frontiers Genet 5:1–14. https://doi.org/10.3389/fgene.2014.00433
Winston ME, Kronauer DJC, Moreau CS (2017) Early and dynamic colonization of Central America drives speciation in Neotropical army ants. Molec Ecol 26:859–870. https://doi.org/10.1111/mec.13846
Yule KM, Koop JAH, Alexandre NM, Johnston LR, Whiteman NK (2016) Population structure of a vector-borne plant parasite. Molec Ecol 25:3332–3343. https://doi.org/10.1111/mec.13693
Acknowledgements
We thank Cristina Bárcenas, Pablo Carrillo, Luis Cervantes✝, Etelvina Gándara, Felicitas Lagunes, José Luis Martínez, María Teresa Mejía-Saules, Eduardo Ruiz-Sanchez and Victoria Sosa who helped in obtaining samples and/or generated sequences for this work; and Ricarda Riina and two anonymous reviewers for useful comments on previous versions of the manuscript. Permission to conduct our fieldwork was granted by the Mexican government (Instituto Nacional de Ecología, Secretaría del Medio Ambiente y Recursos Naturales, SGPA/DGGFS/712/1299/12), and collecting permits from Guatemala (Universidad del Valle, UVAL) and Honduras (Centro Universitario Regional del Litoral Atlántico, CURLA) herbaria. This work was supported by competitive grants (grant numbers 61710, 155686, A1-S-26134) from the Consejo Nacional de Ciencia y Tecnología (CONACyT; http://www.conacyt.mx) and research funds (20030/10563) from the Departamento de Biología Evolutiva, Instituto de Ecología, AC (INECOL) awarded to Juan Francisco Ornelas. Doctoral scholarships from CONACyT were granted to A.E.O.R. (262563), Y.L.V. (262561) and E.A.L.H. (584159), and a research assistant scholarship from CONACyT was granted to M.H.S.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical statement
The authors comply will all rules of the journal following the COPE guidelines; all authors have contributed and approved the final manuscript.
Additional information
Handling Editor: Ricarda Riina.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Information on Electronic Supplementary Material
Information on Electronic Supplementary Material
Online Resource 1. Potential effects of Pleistocene glacial/interglacial cycles on the distribution of suitable habitat for populations of the mistletoe, Psittacanthus rhynchanthus for the last interglacial (LIG, 140–120 ka BP), Last Glacial Maximum (LGM, 21 ka BP) and the present (0 ka).
Online Resource 2. Geographic information and sample sizes of the 22 Psittacanthus rhynchanthus localities sampled in this study.
Online Resource 3. Time divergence estimates and phylogenetic analysis for P. rhynchanthus individuals based on nrDNA and combined cpDNA (trnL-F/atpB-rbcL) sequence data using a Bayesian approach.
Online Resource 4. Numbers of genetically analysed samples (n) for each molecular marker (ITS and trnL-F/atpB-rbcL), and numbers of distinct ribotypes (R) and haplotypes (H) found in Psittacanthus rhynchanthus individuals sampled.
Online Resource 5. Rarefaction analyses for (a) individual- and (b) population-based haplotype richness (95% confidence intervals, CI) accumulation of cpDNA haplotypes based on random sampling of the Psittacanthus rhynchanthus data set.
Online Resource 6. Bayesian skyline plots showing historical demographic trends of Psittacanthus rhynchanthus showing changes in effective population size (Ne; mean ± 95% central posterior density) over time.
Online Resource 7. Factor loadings from the principal components analysis of Psittacanthus rhynchanthus in Mesoamerica on temperature and precipitation variables from WorldClim.
Rights and permissions
About this article
Cite this article
Ortiz-Rodriguez, A.E., Licona-Vera, Y., Vásquez-Aguilar, A.A. et al. Genetic differentiation among Psittacanthus rhynchanthus (Loranthaceae) populations: novel phylogeographic patterns in the Mesoamerican tropical lowlands. Plant Syst Evol 306, 10 (2020). https://doi.org/10.1007/s00606-020-01638-y
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00606-020-01638-y