Advertisement

Phylogeographic patterns and species delimitation in the endangered silverside “humboldtianum” clade (Pisces: Atherinopsidae) in central Mexico: understanding their evolutionary history

  • Isai Betancourt-Resendes
  • Rodolfo Perez-Rodríguez
  • Irene De Los Angeles Barriga-Sosa
  • Kyle R. Piller
  • Omar Domínguez-DomínguezEmail author
Original Article

Abstract

The Atherinopsidae is the second largest group of freshwater fishes occupying central Mexico and is one of biological, cultural, and economic importance. The “humboldtianum” clade (Genus Chirostoma) is a “species flock” of nine described species that inhabit lacustrine ecosystems in central Mexico. The high morphological polymorphism within the group makes species identification difficult and thereby limits the development of research and management projects focusing on this group. In this study, we used phylogeographic and coalescent-based methods to understand the evolution of genetic variation among these species. The results revealed taxonomic inaccuracies and genetic admixture among species. Genetic variation was structured geographically, rather than taxonomically, and five closely related genetic groups were recovered. Two evolutionary pathways were found. First, a novel geographical arrangement of haplotypes was recovered that gave rise to the five recently (Pleistocene, < 1 Myr) derived genetic groups. The second pathway showed a recent intra-lacustrine genetic differentiation that could be associated with sympatric or ecological speciation. The current classification of the group is revised and includes a reduction in the number of valid species in the “humboldtianum” clade. Moreover, this study provides new insight into the biogeography and evolutionary history of this important group of fishes.

Keywords

Species flock Phenotypic plasticity Recent divergences Taxonomic inaccuracy Polymorphism 

Notes

Acknowledgements

IBR would like to thank the Consejo Nacional de Ciencia y Tecnología (CONACyT) for granting a scholarship, and the CIPRES Cyberinfrastructure for Phylogenetic Research XSEDE for their computational support. Conacyt-CB-2009-1-130220 to IDLAB partially funded the specimen sampling. We thank the División de estudios de Posgrado de la Universidad Michoacana de San Nicolás de Hidalgo for funding the English editing of the manuscript. We thank B. García-Andrade, G. Beltrán-López, A. González-Alejo, D. Montejo-Diaz and F. Mar-Silva for their field support.

Funding information

We thank the Coordinación de la Investigación Científica-UMSNH, of Mexico (CIC-2016-18 to ODD) and the National Science Foundation (NSF 1354930 to KRP) for financially funding the project.

Supplementary material

13127_2019_419_MOESM1_ESM.nex (167 kb)
ESM 1 (NEX 167 kb)
13127_2019_419_MOESM2_ESM.nex (38 kb)
ESM 2 (NEX 38.1 kb)
13127_2019_419_MOESM3_ESM.nex (72 kb)
ESM 3 (NEX 71.7 kb)
13127_2019_419_MOESM4_ESM.pdf (110 kb)
ESM 4 (PDF 109 kb)

References

  1. Alarcón-Duran, I., Castillo-Rivero, M. A., Figueroa-Lucero, G., Arroyo-Cabrales, J., Barriga-Sosa I. A., (2017). Diversidad morfológica en 6 poblaciones del pescado blanco Chirostoma humboldtianum. Revista Mexicana de Biodiversidad. 88:207-214.  https://doi.org/10.1016/j.rmb.2017.01.018 CrossRefGoogle Scholar
  2. Alaye, R. N. (1993). El pescado blanco (género Chirostoma) del lago de Pátzcuaro, Michoacán. Composición de especies. Ciencia Pesquera, 9, 113–128.Google Scholar
  3. Alaye, R. N. (1996). Estudios del polimorfismo de la hemoglobina para identificar especies del género Chirostoma del lago de Pátzcuaro, Michoacán, México. Ciencia Pesquera, 13, 1–9.Google Scholar
  4. Álvarez, J. (1972). Ictiología michoacana V. Origen y distribución del a ictiofauna dulceacuícola michoacana. Anales. Escuela Nacional de Ciencias Biológicas, 19, 155–161.Google Scholar
  5. Avise, J. C. (2000). Phylogeography: the history and formation of species. Harvard University Press.Google Scholar
  6. Bandelt, H. J., Forster, P., & Röhl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution, 16, 37–48.  https://doi.org/10.1093/oxfordjournals.molbev.a026036.CrossRefPubMedPubMedCentralGoogle Scholar
  7. Barbour, D. (1973a). A biogeographical history of Chirostoma (Pisces: Atherinidae): a species flock from the Mexican Plateau. Copeia., 3, 533–556.CrossRefGoogle Scholar
  8. Barbour, D. (1973b). The systematics and evolution of the genus Chirostoma Swainson (Pisces, Atherinidae). Talune Studies in Zoology and Botany., 18(3), 97–140.Google Scholar
  9. Barbour, C. D., & Chernoff, B. (1984). Comparative morphology and morphometric of the pescados blancos (genus Chirostoma) from Lake Chapala Mexico. In a Echelle & Kornfield (ed), Evolution of fish species flock. Univ Maine Orono, (pp 111-127).Google Scholar
  10. Barluenga, M., Stölting, K. N., Salzburger, W., Muschick, M., & Meyer, A. (2006). Sympatric speciation in Nicaraguan crater lake cichlid fish. Nature, 439, 719–723.  https://doi.org/10.1038/nature04325.CrossRefPubMedGoogle Scholar
  11. Barriga-Sosa, I., Ibáñez-Aguirre, A. L., & Arredondo-Figueroa, J. L. (2002). Morphological and genetic variation in seven species of the endangered Chirostomahumboldtianum species group” (Atheriniformes: Atherinopsidae). Revista de Biología Tropical, 50, 199–216.Google Scholar
  12. Barriga-Sosa, I., Eguiarte, L. E., & Arredondo-Figueroa, J. L. (2004). Low but significant subdivision among populations of Chirostoma grandocule from Lake Patzcuaro, México. Biotropica, 36, 85–98.  https://doi.org/10.1111/j.1744-7429.2004.tb00299.x.CrossRefGoogle Scholar
  13. Barriga-Sosa, I., García-De Leon, F., & Del Río-Portillam M.A. (2014). The complete mitochondrial DNA of the endemic shortfin silverside, Chirostoma humboldtianum (Valenciennes, 1835). Journal of Mitochondrial DNA Part A, 27:2, 1545-1546.  https://doi.org/10.3109/19401736.2014.953130.CrossRefGoogle Scholar
  14. Barriga-Sosa, I., Pérez-Ramírez, M. Y., Soto-Aguirre, F., Castillo-Rivera, M., & Arredondo-Figueroa, J. L. (2005). Inter-specific variation of the mitochondrial r16S gene among silversides, “Peces Blancos”, (Atherinopsidae: Menidiinae) and its utilization for species identification. Aquaculture, 250, 637–651.  https://doi.org/10.1016/j.aquaculture.2005.05.003.CrossRefGoogle Scholar
  15. Beltrán-López, R. G., Domínguez-Domínguez, O., Guerrero, J. A., Corona-Santiago, D. K., Mejía-Mojica, H., & Doadrio, I. (2017). Phylogeny and taxonomy of the genus Ilyodon Eigenmann, 1907 (Teleostei: Goodeidae), based on mitochondrial and nuclear DNA sequences. Journal of Zoological Systematics and Evolutionary Research, 1907.  https://doi.org/10.1111/jzs.12175.CrossRefGoogle Scholar
  16. Beltrán-López, R. G., Domínguez-Domínguez, O., Pérez-Rodríguez, R., Kyle, P., & Doadrio, I. (2018). Envolving in the highlands: the case of the Neotropical Lerma live-bearing Poeciliopsis infans (Wolman, 1984) (Cyprinodontiformes: Poeciliidae) in Central Mexico. BMC Evololutionary Biology, 18, 56.  https://doi.org/10.1186/s12862-018-1172-7.CrossRefGoogle Scholar
  17. Betancourt-Resendes, I., Pérez-Rodríguez, R., & Domínguez-Domínguez, O. (2018). Speciation of silverside Chirostoma attenuatum (Pisces: Atheriniformes) in Central Mexico. Journal of Zoological Systematics and Evolutionary Research. 00:1-12. doi.org/ https://doi.org/10.1111/jzs.12216.CrossRefGoogle Scholar
  18. Bloom, D. D., Piller, K. R., Lyons, J., Mercado-Silva, N., & Medina-Nava, M. (2009). Systematics and biogeography of the silverside tribe Menidiini (Teleostomi: Atherinopsidae) based on the mitochondrial ND2 gene. Copeia., 2009, 408–417.  https://doi.org/10.1643/CI-07-151.CrossRefGoogle Scholar
  19. Bloom, D. D., Unmack, P. J., Gosztonyi, A. E., Piller, K. R., & Lovejoy, N. R. (2012). It’s a family matter: molecular phylogenetics of Atheriniformes and the polyphyly of the surf silversides (family: Notocheiridae). Molecular Phylogenetics and Evolution, 62, 1025–1030.  https://doi.org/10.1016/j.ympev.2011.12.006.CrossRefPubMedGoogle Scholar
  20. Bloom, D. D., Weir, J. T., Piller, K. R., & Lovejoy, N. R. (2013). Do freshwater fishes diversify faster than marine fishes? A test using state-dependent diversification analyses and molecular phylogenetics of new world silversides (atherinopsidae). Evolution, 67, 2040–2057.  https://doi.org/10.1111/evo.12074.CrossRefPubMedPubMedCentralGoogle Scholar
  21. Campanella, D., Hughes, L. C., Unmack, P. J., Bloom, D. D., Piller, K. R., & Ortí, G. (2015). Multi-locus fossil-calibrated phylogeny of Atheriniformes (Teleostei, Ovalentaria). Molecular Phylogenetics and Evolution, 86, 8–23.  https://doi.org/10.1016/j.ympev.2015.03.001.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Caviedes-Solis, I. W., & Nieto-Montes de Oca, A. (2018). A multilocus phylogeny of the genus Sarcohyla (Anura: Hylidae), and an investigation of species boundaries using statistical species delimitation. Molecular Phylogenetics and Evolution, 118, 184–193.  https://doi.org/10.1016/j.ympev.2017.09.010.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Chernoff, B. (1982). Character variation among populations and the analysis of biogeography. American Zoology, 22, 425–439.CrossRefGoogle Scholar
  24. Chow, S., & Hazama, K. (1998). Universal PCR primers for S7 ribosomal protein gene introns in fish. Molecular Ecology, 7, 1247–1263.CrossRefGoogle Scholar
  25. Corona-Santiago, D. K., Doadrio, I., & Domínguez-Domínguez, O. (2015). Evolutionary history of the live-bearing andemic Allotoca diazi species complex (Actinopterygii, Goodeinae): evidence of founder effect events in the Mexican Pre-hispanic period. PLoS One, 10, e0124138.  https://doi.org/10.1371/journal.pone.0124138.CrossRefPubMedPubMedCentralGoogle Scholar
  26. De Buen, F. (1943). Los lagos michoacanos. I. Caracteres generales el Lago de Zirahuén. Revista de la Sociedad Mexicana de Historia Natural, 4, 211–232.Google Scholar
  27. Doadrio, I., & Domínguez, O. (2004). Phylogenetic relationships within the fish family Goodeidae based on cytochrome b sequence data. Molecular Phylogenetics and Evolution, 31, 416–430.  https://doi.org/10.1016/j.ympev.2003.08.022.CrossRefPubMedGoogle Scholar
  28. Dominguez-Dominguez, O., Doadrio, I., & Perez-Ponce de León, G. (2006). Historical biogeography of some river basins in central México evidenced by their goodeine freshwater fishes: a preliminary hypothesis using secondary Brooks parsimony analysis. Journal of Biogeography, 33, 1437–1447.  https://doi.org/10.1111/j.1365-2699.2006.01526.x.CrossRefGoogle Scholar
  29. Domínguez-Domínguez, O., Alda, F., Pérez-Ponce De León G., García-Garitagoitia, J. L, & Doadrio, I. (2008). Evolutionary history of the endangered fish Zoogoneticus quitzeoensis (Bean, 1898) (Cyprinodontiformes: Goodeidae) using a sequential approach to phylogeography based on mitochondrial and nuclear DNA data. BMC Evolutionary Biology, 8: 161. doi: https://doi.org/10.1186/1471-2148-8-161.PubMedPubMedCentralCrossRefGoogle Scholar
  30. Domínguez-Domínguez, O., Pedraza-Lara, C., Gurrola-Sánchez, N., Perea, S., Pérez-Rodríguez, R., Israde-Alcántara, I., et al. (2010). Historical biogeography of the Goodeinae (Cyprinodontiforms). In: Uribe MC, Grier HJ. (Ed.) Viviparous Fishes II. (pp. 34–69). New life publications 2010.Google Scholar
  31. Drummond, A. J., & Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology.  https://doi.org/10.1186/1471-2148-7-214.PubMedPubMedCentralCrossRefGoogle Scholar
  32. Drummond, A. J., Rambaut, A., Shapiro, B., & Pybus, O. G. (2005). Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution, 22, 1185–1192.  https://doi.org/10.1093/molbev/msi103.CrossRefPubMedPubMedCentralGoogle Scholar
  33. Echelle, A. A., Echelle, A. F. (1984). Evolutionary genetics of a “species flock” Atherinid fishes on mesa central of Mexico. In an Echelle & Kornfield. (Ed.) Evolution of fish species flock, (pp 93-110). University Maine Orono.Google Scholar
  34. Elmer, K. R., Kusche, H., Lehtonen, T. K., & Meyer, A. (2010). Local variation and parallel evolution: morphological and genetic diversity across a species complex of neotropical crater lake cichids fishes. Philosophical Transaction Royal Society B, 365, 1763–1782.  https://doi.org/10.1098/rstb.2009.0271.CrossRefGoogle Scholar
  35. Excoffier, L., & Lischer, H. E. (2010). Arlequin suite ver 3.5: A new series of programs to perform population genetics analysis under Linux and Windows. Molecular Ecology Resources, 10, 564–567. doi: org/ https://doi.org/10.1111/j.1755-0998.2010.02847.x.
  36. Excoffier, L., Smouse, P. E., & Quattro, J. M. (1992). Analysis of molecular variance inferred from metric distance among DNA haplotypes application to human mitochondrial DNA restriction data. Genetics, 131, 479–491.PubMedPubMedCentralGoogle Scholar
  37. Fluker, B. L., Pezold, F., & Minton, R. L. (2011). Molecular and morphological divergence in the inland silverside (Menidia beryllina) along a freshwater-estuarine interface. Enviromental Biolology of Fishes, 91, 311–325.  https://doi.org/10.1007/s10641-011-9786-2.CrossRefGoogle Scholar
  38. García-de León, F. J., Ramírez-Herrejón, J. P., García-Ortega, R., & Hendrickson, D. A. (2014). Foraging patterns of four sympatric species of silversides (Atheriniformes: Atherinopsidae) in Lago de Pátzcuaro , Central México. UNED Research Journal, 6, 127–139.CrossRefGoogle Scholar
  39. García-Martínez, R. M., Mejía, O., García-De Leon, F. J., & Barriga-Sosa, I. (2015). Extreme genetics divergence in the endemic fish Chirostoma humboldtianum ( Valenciennes , 1835 ): implications for its conservation. Hidrobiológica, 25, 95–106.Google Scholar
  40. Garduño-Monroy, V. H., Chávez-Hernández, J., Aguirre-González, J., Vázquez-Rosas, R., Mijares, H., Israde-Alcántara, I., et al. (2009). Zonificación de los periodos naturales de oscilación superficial en la ciudad de Pátzcuaro, Mich. México, con base en microtremores y estudios paleosismología. Revista Mexicana de Ciencias Geológicas, 26, 623–637.Google Scholar
  41. Grummer, J. A., Bryson Jr., R. W., & Reeder, T. W. (2014). Species delimitation using Bayes factors: simulations and application to the Sceloporus scalaris species group (Squamata: Phrynosomatidae). Systematic Biology, 63, 119–133.  https://doi.org/10.1093/sysbio/syt069.CrossRefPubMedGoogle Scholar
  42. Gulisija, D., Kim, Y., & Plotkin, J. B. (2016). Phenotypic plasticity promotes balanced polymorphism in periodic environments by a genomic storage effect. Genetics., 202, 1437–1448.  https://doi.org/10.1101/038497.CrossRefPubMedPubMedCentralGoogle Scholar
  43. Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580.  https://doi.org/10.1093/molbev/msp274.CrossRefPubMedGoogle Scholar
  44. Israde-Alcántara, I., & Garduño-Monroy, V. H. (1999). Lacustrine record in a volcanic intra-arc setting: the evolution of the late Neogene Cuitzeo basin system (central-western Mexico, Michoacan). Palaeogeography, Palaeoclimatology, Palaeoecology, 151, 209–227.CrossRefGoogle Scholar
  45. Israde-Alcántara, I., Garduño-Monroy, V. H., Fisher, C. T., Pollard, H. P., & Rodríguez-Pascua, M. A. (2005). Lake level change, climate, and the impact of natural events: the role of seismic and volcanic events in the formation of the Lake Patzcuaro Basin, Michoacan, México. Quaternary International, 135, 35–46.  https://doi.org/10.1016/j.quaint.2004.10.022.CrossRefGoogle Scholar
  46. Kass, R. E., & Raftery, A. E. (1995). Bayes factors. Journal of the American Statistical Association, 90, 773–795.CrossRefGoogle Scholar
  47. Lake, C., Rodriguez-ruiz, A., & Granado-lorencio, C. (1988). Características del aparato bucal asociadas al régimen alimenticio en cinco especies coexistentes del género Chirostoma (Lago de Chapala, México). Revista Chilena de Historia Natural, 61, 35–51.Google Scholar
  48. Lanfear, R., Calcott, B., Ho, S. Y., & Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyzes. Molecular Biology and Evolution, 29, 1695–1701.PubMedCrossRefPubMedCentralGoogle Scholar
  49. Lartillot, N., & Philippe, H. (2006). Computing Bayes factors using thermodynamic integration. Systematic Biology, 55, 195–207.PubMedCrossRefPubMedCentralGoogle Scholar
  50. Leaché, A. D., Fujita, M. K., Minin, V. N., & Bouckaert, R. R. (2014). Species delimitation using genome-wide SNP Data. Systematic Biology, 63, 534–542.  https://doi.org/10.1093/sysbio/syu018.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Lee, W. J., Conroy, J., Huntting, W., & Kocher, T. D. (1995). Structure and evolution of teleost mitochondrial control regions. Journal of Molecular Evolution, 42, 54–66.Google Scholar
  52. Librado, P., & Rozas, J. (2009). DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25, 1451–1452.  https://doi.org/10.1093/bioinformatics/btp187.CrossRefPubMedPubMedCentralGoogle Scholar
  53. Maio, N., De Wu. C., Reilly, K. M. O., & Wilson, D., (2015). New Routes to Phylogeography : A Bayesian Structured Coalescent Approximation. PLoS Genetic, 1–22 doi: https://doi.org/10.1371/journal.pgen.1005421.PubMedPubMedCentralCrossRefGoogle Scholar
  54. Mayer, B., & Matschiner, W. (2015). Molecular phylogenetics and evolution a tribal level phylogeny of Lake Tanganyika chichlid fishes based on a genomic multi-marker aproach. Molecular Phylogentics and Evolution, 83, 56–71.  https://doi.org/10.1016/j.ympev.2014.10.009.CrossRefGoogle Scholar
  55. Mayr, E. (1942). Systematics and the origin of species. New York: Columbia University Press.Google Scholar
  56. Mercado-Silva, N., Lyons, J., Moncayo-Estrada, R., Gesundheit, P., Krabbenhoft, T. J., Powell, D. L., & Piller, K. R., (2015). Stable isotope evidence for trophic overlap of sympatric Mexican Lake Chapala silversides (Teleostei: Atherinopsidae: Chirostoma spp.). Neotropical Ichthyolgy, 00–00. doi: https://doi.org/10.1590/1982-0224-20140079.CrossRefGoogle Scholar
  57. Miller, R. R., Minckley, W. L., & Norris, S. M. (2005). Freshwater fishes of Mexico. Chicago: The University of Chicago Press.Google Scholar
  58. Miller, M. A., Schwartz, T., Pickett, B. E., He, S., Klem, E. B., Scheuermann, R. H., Passarotti, M., Kaufman, S., & O’Leary, M. A. (2015). A RESTful API for access to phylogenetic tools via the CIPRES Science Gateway. Evolutionary Bioinformatics, 11, 43–48.  https://doi.org/10.4137/EBO.S21501.CrossRefGoogle Scholar
  59. Moncayo-Estrada, R., & Buelna-Osben, H. R. (2001). Fish fauna of Lake Chapala. In A. M. Hansen & M. van Afferden (Eds.), The Lerma-Chapala watershed. Evaluation and management (pp. 215–242). New York (NY): Kluwer Academic Press.CrossRefGoogle Scholar
  60. Moncayo-Estrada, R., Lyons, J., Escalera-Gallardo, C., & Lind, O. T. (2012). Long-term change in the biotic integrity of a shallow tropical lake: a decadal analysis of the Lake Chapala fish community. Lake and Reservoir Management, 28, 92–104.  https://doi.org/10.1080/07438141.2012.661029.CrossRefGoogle Scholar
  61. Ornelas-García, C. P., Domínguez-Domínguez, O., & Doadrio, I. (2008). Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actinopterygii, Characidae) in Mesoamerica reveals multiple morphological homoplasies. BMC Evolutionary Biology, 8, 340.  https://doi.org/10.1186/1471-2148-8-340.CrossRefPubMedPubMedCentralGoogle Scholar
  62. Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L., Grabosky, G., & Stice, L. (1991). Simple fool’s guide to PCR, version 2. Honolulu, HI: Department of Zoology, University of Hawaii.Google Scholar
  63. Perdices, A., Bermingham, E., Montilla, A., & Doadrio, I. (2002). Evolutionary history of the genus Rhamdia (Teleostei: Pimelodidae) in Central America. Molecular Phylogenetics and Evolution, 25, 172–189.  https://doi.org/10.1016/S1055-7903(02)00224-5.CrossRefPubMedPubMedCentralGoogle Scholar
  64. Pérez-Miranda, F., Mejía, O., Soto-Galera, E., Espinosa-Pérez, H., Piálek, L., & Říčan, O. (2017). Phylogeny and species diversity of the genus Herichthys (Teleostei: Cichlidae). Journla of Zoological Systematic and Evolutionary Research.  https://doi.org/10.1111/jzs.12197.CrossRefGoogle Scholar
  65. Pérez-Rodríguez, R., Domínguez-Domínguez, O., Doadrio, I., Cuevas-García, E., & Pérez-Ponce de Leon, G. (2015). Comparative historical biogeography of three groups of Neartic freshwater fishes across central Mexico. Fish Biology 86, 993-1015.Google Scholar
  66. Pérez-Rodríguez, R., Domínguez-Domínguez, O., Pérez-Ponce de León, G., & Doadrio, I. (2009). Phylogenetic relationships and biogeography of the genus Algansea Girard (Cypriniformes: Cyprinidae) of central México inferred from molecular data. BMC Evolutionary Biology.  https://doi.org/10.1186/1471-2148-9-223. PubMedPubMedCentralCrossRefGoogle Scholar
  67. Piller, K. R., Kenway-Lynch, C. S., Camak, D. T., & Domínguez-Domínguez, O. (2015). Phylogeography and population structure of the imperiled redtail splitfin (Goodeidae: Xenotoca eiseni): Implication for conservation. Copeia.  https://doi.org/10.1643/CI-14-067.CrossRefGoogle Scholar
  68. Rannala, B., & Yang, Z. (2003). Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics, 164, 1645–1656.PubMedPubMedCentralGoogle Scholar
  69. Ribbink, A. J. (1984). Is the species flock concept tenable? In I. Kornfield (Ed.), Echelle AA (pp. 21–25). Orono: Evolution of fish species flocks. University of Maine at Orono Press.Google Scholar
  70. Rosenblum, E. B., Parent, C. E., & Brandt, E. E. (2014). The molecular basis of phenotypic convergence. Annual Review of Ecology, Evolution, and Systematics.  https://doi.org/10.1146/annurev-ecolsys-120213-091851. CrossRefGoogle Scholar
  71. Sambrook, J., Fritsch, E. F., & Maniatis, T. (1989). Molecular cloning: a laboratory manual (2nd ed.). New York, NY: Cold Spring Harbor Laboratory.Google Scholar
  72. Schluter, D. (2000). The ecology of adaptive radiation. Oxford Unversity Press.Google Scholar
  73. Schluter, D., & Conte, G. L. (2009). Genetics and ecological speciation. PNAS.  https://doi.org/10.1073/PNAS.0901264106.CrossRefGoogle Scholar
  74. Seehausen, O. (2004). Hybridization and adaptive radiation. Trends in Ecology & Evolution, 19, 198–207.CrossRefGoogle Scholar
  75. Seehausen, O., & Wagner, C. E. (2014). Speciation in freshwater fishes. Annual Review of Ecology, Evolution, and Systematics.  https://doi.org/10.1146/annurev-ecolsys-120213-091818.CrossRefGoogle Scholar
  76. Soria-Barreto, M., & Paulo-Maya, J. (2005). Morfometría comparada del aparato mandibular en especies de Chirostoma Atheriniformes : Atherinopsidae del Lago de Pátzcuaro , Michoacán , México Morphometric comparison of the mandibular region in species of Chirostoma Atheriniformes : Atherinopsid. Hidrobiologica, 15, 161–168.Google Scholar
  77. Tamura, K., Stecher, G., Peterson, D., Filipski, A., & Kumar, S. (2013). MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution.  https://doi.org/10.1093/molbev/mst197.PubMedPubMedCentralCrossRefGoogle Scholar
  78. Tarvin, R. D., Powell, E. A., Santos, J. C., Ron, S. R., & Cannatella, D. C. (2017). The birth of aposematism: high phenotypic divergence and low genetic diversity in a young clade of poison frogs. Molecular Phylogenetics and Evolution.  https://doi.org/10.1016/j.ympev.2016.12.035.PubMedCrossRefPubMedCentralGoogle Scholar
  79. Thompson, D. J., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The Clustal_X windows interface: flexible strategies for multiple sequences alignment aided by quality analysis tools. Nucleic Acids Research.  https://doi.org/10.1093/nar/25.24. 4876.
  80. Unmack, P. J., Allen, G. R., & Johnson, J. B. (2013). Phylogeny and biogeography of rainbowfishes (Melanotaeniidae) from Australia and New Guinea. Molecular Phylogenetics and Evolution.  https://doi.org/10.1186/s12862-018-1172-7.
  81. Wagner, C. E., Keller, I., Wittwer, S., Selz, O. M., Mwaiko, S., Greuter, L., Sivasundar, A., & Seehausen, O. (2012). Genome-wide RAD sequences data provide unprecedented resolution of species bundaries and relathionships in the Lake Victoria chichlid adaptaive radiation. Molecular Ecolology.  https://doi.org/10.1111/mec.12023.PubMedCrossRefGoogle Scholar
  82. Wainwright, P., Smith, W., & Price, S. (2012). The evolution of pharyngognathy: a phylogenetic and functional appraisal of the pharyngeal jaw key innovation in labroid fishes and beyond. Systematic Biology.  https://doi.org/10.1093/sysbio/sys060.PubMedCrossRefGoogle Scholar
  83. Ward, R. D., Woodwark, M., & Skibinski, D. O. F. (1994). A comparison od genetic diversity levels in marine, freshwater, and anadramous fishes. Journal of Fish Biology, 44, 213–232.CrossRefGoogle Scholar
  84. Xia, X. (2013). DAMBE5: a comprehensive softwere package for data analysis in molecular biology and evolution. Molecular Biology and Evolution.  https://doi.org/10.1093/molbev/mst064.PubMedPubMedCentralCrossRefGoogle Scholar
  85. Xie, W. G., Lewis, P. O., Fan, Y., Kuo, L., & Chen, M. H. (2011). Improving marginal likelihood estimation for Bayesian phylogenetic model selection. Systematic Biology.  https://doi.org/10.1093/sysbio/syq085.PubMedPubMedCentralCrossRefGoogle Scholar
  86. Yang, Z. (2015). The BPP program for species tree estimation and species delimitation. Current Zoology, 61(5), 854–865.  https://doi.org/10.1093/czoolo/61.5.854.CrossRefGoogle Scholar
  87. Yang, Z., & Rannala, B. (2010). Bayesian species delimitation using multilocus sequence data. PNAS.  https://doi.org/10.1073/pnas.0913022107.CrossRefGoogle Scholar
  88. Yang, Z., & Rannala, B. (2014). Unguided species delimitation using DNA sequence data from multiple loci. Molecular Biology and Evolution.  https://doi.org/10.1093/molbev/msu279.PubMedPubMedCentralCrossRefGoogle Scholar
  89. Yoder, J. B., Clacey, E., Des Roches, S., Eastman, J. M., Gentry, L., Godsoe, W., Hagey, T. J., Jochimsen, D., Oswald, B. P., Robertson, J., Sarver, B. A. J., Schenk, J. J., Spear, S. F., & Harmon, L. J. (2010). Ecological opportunity and the origen of adaptative radiations. Evolutionary Biology.  https://doi.org/10.1111/j.1420-9101.2010.02029.x.PubMedCrossRefPubMedCentralGoogle Scholar
  90. Zamudio, K. R., Bel, R. C., & Mason, N. A. (2016). Phenotypes in phylogeography: species’ traits, environmental variation, and vertebrate diversification. PNAS.  https://doi.org/10.1073/pnas.1602237113.CrossRefGoogle Scholar

Copyright information

© Gesellschaft für Biologische Systematik 2019

Authors and Affiliations

  • Isai Betancourt-Resendes
    • 1
    • 2
  • Rodolfo Perez-Rodríguez
    • 3
    • 4
  • Irene De Los Angeles Barriga-Sosa
    • 5
  • Kyle R. Piller
    • 6
  • Omar Domínguez-Domínguez
    • 3
    • 4
    Email author
  1. 1.Programa Institucional de Doctorado en Ciencias Biológicas, Facultad de BiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico
  2. 2.CONACYT-Facultad de Ciencias NaturalesUniversidad Autónoma de QuerétaroSantiago de QuerétaroMéxico
  3. 3.Laboratorio de Biología Acuática, Facultad de BiologíaUniversidad Michoacana de San Nicolás de HidalgoMoreliaMéxico
  4. 4.Laboratorio Nacional de Análisis y Síntesis Ecológica para la Conservación de Recursos Genéticos de México, Escuela Nacional de Estudios SuperioresUnidad Morelia, Universidad Nacional Autónoma de MéxicoMoreliaMéxico
  5. 5.Laboratorio de Genética y Biología Molecular de la Planta Experimental de Producción Acuícola Departamento de HidrobiologíaUniversidad Autónoma Metropolitana Unidad IztapalapaMéxicoMéxico
  6. 6.Department of Biological SciencesSoutheastern Louisiana UniversityHammondUSA

Personalised recommendations