Conservation Genetics

, Volume 15, Issue 2, pp 483–488 | Cite as

Conservation genetic assessment of the critically endangered Julimes pupfish, Cyprinodon julimes

  • Evan W. CarsonEmail author
  • Mauricio De la Maza-Benignos
  • María de Lourdes Lozano-Vilano
  • Lilia Vela-Valladares
  • Iris Banda-Villanueva
  • Thomas F. Turner
Short Communication


Pupfishes (genus Cyprinodon) are iconic of biodiversity and endemism in the desert southwest of North America. Most of these species are imperiled, primarily because of excessive exploitation of water resources in this arid region. The critically endangered Julimes pupfish, Cyprinodon julimes, is restricted to a small, isolated, and highly modified desert spring in Chihuahua, México. We evaluated effective population size (microsatellites) and genetic variation (microsatellites and mitochondrial DNA) to determine the conservation genetic status of this species. The effective population size was critically low and indicated that this pupfish is at genetic risk of extinction through loss of adaptive variance and, potentially, from inbreeding depression. Mitochondrial variation was also extremely low, and haplotype frequency was biased heavily in favor of one of two variants. The uncommon haplotype was derived from a past hybridization event with the closely related C. eximius; whether cessation of introgressive hybridization is relevant to conservation management of Julimes pupfish is unknown but may be important to consider. Minimally, C. julimes is compromised genetically. Baseline population genetic information provided by this study will be vital to long-term monitoring of this highly imperiled species.


Cyprinodon julimes Effective population size Genetic diversity Introgression Population bottleneck Endangered species 



We thank Hailey Conover for assistance in the laboratory; for curatorial assistance, we thank Alexandra Snyder, Collection Manager, Division of Fishes, Museum of Southwestern Biology, University of New México. We extend special thanks to Amigos del Pandeño, A. C., for their invaluable participation and partnership. Pronatura Noreste, A. C., provided funding. Specimens were obtained in accordance with permits provided under Oficio SGPA/DGVS/02833/12 to Ma. De Lourdes Lozano-Vilano. The photograph of a breeding male Julimes pupfish was taken by Juan Miguel Artigas Azas for De la Maza-Benignos (editor). De la Maza-Benignos De la Maza-Benignos and De la Maza-Benignos 2009. Los Peces del Río Conchos. Alianza WWF-Fundación-Gonzalo Río Arronte y Gobierno del Estado de Chihuahua.


  1. Alò D, Turner TF (2005) Effect of habitat fragmentation on effective population size in the endangered rio grande silvery minnow. Conserv Biol 19:1138–1148CrossRefGoogle Scholar
  2. Avise JC (1996) Introduction: the scope of conservation genetics. In: Avise JC, Hamrick J (eds) Conservation genetics: case histories from nature. Chapman & Hall, New York, pp 1–9Google Scholar
  3. Carson EW, Dowling TE (2006) Influence of hydrogeographic history and hybridization on the distribution of genetic variation in the pupfishes Cyprinodon atrorus and C. bifasciatus. Mol Ecol 15:667–679PubMedCrossRefGoogle Scholar
  4. Carson EW, Tobler M, Minckley WL, Ainsworth RJ, Dowling TE (2012) Relationships between spatio-temporal environmental and genetic variation reveal an important influence of exogenous selection in a pupfish hybrid zone. Mol Ecol 21:1209–1222PubMedCrossRefGoogle Scholar
  5. Carson EW, Beasley RR, Jones KL, Lance SL, De Ma Lozano-Vilano L, Vela-Valladares L, Banda-Villanueva I, Turner TF, De la Maza-Benignos M (2013a) Development of polymorphic microsatellite markers for the microendemic pupfishes Cyprinodon julimes and C. pachycephalus. Conserv Genet Resour 5:853–856CrossRefGoogle Scholar
  6. Carson EW, Espinosa-Pérez H, Souza V (2013b) Low mitochondrial DNA sequence variation in the microendemic Cuatro Ciénegas platy fish Xiphophorus gordoni. West N Am Naturalist 73:224–229CrossRefGoogle Scholar
  7. Contreras-Balderas S, De Lozano-Vilano ML (1996) Extinction of most sandia and potosí valleys (Nuevo León, México) endemic pupfishes, crayfishes, and snails. Ichthyol Explor Freshw 7:33–40Google Scholar
  8. Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics, and parallel computing. Nat Methods 9:772PubMedCrossRefGoogle Scholar
  9. De la Maza-Benignos M (2009) Presentación. In: De la Maza-Benignos M (ed) Los Peces del Río Conchos. Alianza WWF-Fundación Gonzalo Río Arronte, I.A.P. y Gobierno del Estado de Chihuahua, México, pp 9–12Google Scholar
  10. De la Maza-Benignos M, Vela-Valladares L (2009) Cyprinodon julimes sp. nov. In: De la Maza-Benignos M (ed) Los Peces del Río Conchos. Alianza WWF-Fundación Gonzalo Río Arronte, I.A.P. y Gobierno del Estado de Chihuahua, México, pp 185–189Google Scholar
  11. De la Maza-Benignos M, Rodriguez-Pineda JA, De la Mora-Covarrubias A, Carson EW, Quiñones-Martínez M, Lavín-Murcio P, Vela-Valladares L, Lozano-Vilano Ma de L, Parra-Gallo H, Macías-Duarte A, Lebgue-Keleng T, Pando-Pando E, Pando-Pando M, Andazola-González M, Anchondo-Najera A, Quintana-Martínez G, Zapata-López J, Banda-Villanueva IA, Ibarrola-Reyes HJ (2012) Planes de Manejo y Programa de Monitoreo de Signos Vitales para las Áreas de Manantiales de la UMA El Pandeño; y San Diego de Alcalá en el Desierto Chihuahuense. Vol 1. Pronatura Noreste, A. C. Amigos del Pandeño, A. C.Google Scholar
  12. Echelle AA, Echelle AF, Contreras-Balderas S, Ma de L Lozano-Vilano(2001) Pupfishes of the Northern Chihuahuan Desert: status and conservation. Aquatic Fauna of the Northern Chihuahuan Desert, contributed papers from a special session within the thirty-third annual symposium of the Desert Fishes Council. Special Publications, Museum of Texas Tech University, vol 46, pp 111–126Google Scholar
  13. Echelle AA, Carson EW, Echelle AF, Van Den Bussche RA, Dowling TE, Meyer A (2005) Historical biogeography and the role of genetic introgression in the evolution of the new world pupfish genus Cyprinodon (Teleostei: Cyprinodontiformes). Copeia 2005:320–339CrossRefGoogle Scholar
  14. Excoffier L, Lischer HEL (2010) Arlequin suite ver. 3.5: a new series of program to perform population genetics analyses under linux and windows. Mol Ecol Resour 10:564–567PubMedCrossRefGoogle Scholar
  15. Franklin IR (1980) Evolutionary change in small populations. In: Soule ME, Wilcox BA (eds) Conservation biology: an evolutionary-ecology perspective. Sinauer Associates, Sunderland, pp 138–148Google Scholar
  16. Gold JR, Saillant E, Burridge CP, Blanchard A, Patton JC (2004) Population structure and effective size in critically endangered cape fear shiners Notropis mekistocholas. Southeast Nat 3:89–102CrossRefGoogle Scholar
  17. Guidon S, Gascuel O (2003) A simple, fast, and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 5:696–704CrossRefGoogle Scholar
  18. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162CrossRefGoogle Scholar
  19. Hershler R, Liu H-P, Landye J (2011) New species and records of springsnails (Caenogastropoda: Cochliopidae: Tryonia) from the Chihuahuan desert (México and United States), an imperiled biodiversity hotspot. Zootaxa 3001:1–32Google Scholar
  20. Kallman KD (1964) Genetics of tissue transplantation in isolated platy fish populations. Copeia 1964:513–522CrossRefGoogle Scholar
  21. Koike H, Echelle AA, Loftis D, Van Den Bussche RA (2008) Microsatellite DNA analysis of success in conserving genetic diversity after 33 years of refuge management for the desert pupfish complex. Anim Conserv 11:321–329CrossRefGoogle Scholar
  22. Martin A, Wilcox JL (2004) Evolutionary history of ash meadows pupfish (genus Cyprinodon) populations inferred using microsatellite markers. Conserv Genet 5:769–782CrossRefGoogle Scholar
  23. Miller RR, Minckley WL, Norris S (2005) Freshwater fishes of México. University of Chicago Press, ChicagoGoogle Scholar
  24. Minckley WL, Marsh PC (2002) Inland fishes of the greater southwest: chronicle of a vanishing biota. University of Arizona Press, TucsonGoogle Scholar
  25. Minckley WL, Minckley CO (1986) Cyprinodon pachycephalus, a new species of pupfish (Cyprinodontidae) from the Chihuahuan desert of northern México. Copeia 1986:184–192CrossRefGoogle Scholar
  26. Minckley WL, Meffe GK, Soltz DL (1991) Conservation and management of short-lived fishes: the cyprinodontoids. In: Minckley WL, Deacon JE (eds) Battle against extinction: native fish management in the American West. Univ. of Arizona Press, Tucson, pp 247–282Google Scholar
  27. Osborne MJ, Davenport SR, Hoagstrom CW, Turner TF (2010) Genetic effective size, N e, tracks density in a small freshwater cyprinid, pecos bluntnose shiner (Notropis simus pecosensis). Mol Ecol 19:2832–2844PubMedCrossRefGoogle Scholar
  28. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  29. Reyes I (2009) Reconocimiento geomorfológico del área de Julimes, Chihuahua. World Wildlife Fund, Chihuahuan Desert Program and Facultad de Ingeniería de laUniversidad Autónoma de Chihuahua, MéxicoGoogle Scholar
  30. Rieman BE, Allendorf FW (2001) Effective population size and genetic conservation criteria for bull trout. N Am J Fish Manage 21:756–764CrossRefGoogle Scholar
  31. Rodríguez-Ramírez A, Ballesteros-Barrera C (2009) Estudio paleoambiental del área “El Pandeño”, Julimes. Chihuahua, Facultad de Ciencias de la UNAM for World Wildlife FundGoogle Scholar
  32. Saillant E, Patton JC, Ross KE, Gold JR (2004) Conservation genetics and demographic history of the endangered Cape Fear shiner (Notropis mekistocholas). Mol Ecol 13:2947–2958PubMedCrossRefGoogle Scholar
  33. Salgueiro P, Carvalho G, Collares-Pereira MJ, Coelho MM (2003) Microsatellite analysis of genetic population structure of the endangered cyprinid Anaecypris hispanica in Portugal: implications for conservation. Biol Conserv 109:47–56CrossRefGoogle Scholar
  34. Schmidt TR, Bielawski JP, Gold JR (1998) Molecular phylogenetics and evolution of the cytochrome b gene in the cyprinid genus Lythrurus (Actinopterygii: Cypriniformes). Copeia 1998:14–22CrossRefGoogle Scholar
  35. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33PubMedCrossRefGoogle Scholar
  36. SEMARNAT (2012) Fomento a la Conservación y al Aprovechamiento Sustentable de la Vida Silvestre 08D01-00025/1201 Amigos del Pandeño, A.C. under Lineamientos para obtener subsidios de fomento a la conservación y aprovechamiento sustentable de la vida silvestre en UMA o PIMVS en las comunidades rurales de la República Mexicana. Ejercicio 2012Google Scholar
  37. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731–2739PubMedCentralPubMedCrossRefGoogle Scholar
  38. Tibbets CA, Dowling TE (1996) Effects of intrinsic and extrinsic factors on population fragmentation in three species of north American minnows (Teleostei: Cyprinidae). Evolution 50:1280–1292CrossRefGoogle Scholar
  39. Tobler M, Carson EW (2010) Environmental variation, hybridization, and phenotypic diversification in Cuatro Ciénegas pupfishes. J Evol Biol 23:1475–1489PubMedCrossRefGoogle Scholar
  40. Turner BJ, Liu RK (1977) Extensive interspecific genetic compatibility in the new world killifish genus Cyprinodon. Copeia 1977:259–269CrossRefGoogle Scholar
  41. Waples RS, Do C (2008) LDNE: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756PubMedCrossRefGoogle Scholar
  42. Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262PubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Evan W. Carson
    • 1
    Email author
  • Mauricio De la Maza-Benignos
    • 2
  • María de Lourdes Lozano-Vilano
    • 3
  • Lilia Vela-Valladares
    • 2
  • Iris Banda-Villanueva
    • 2
  • Thomas F. Turner
    • 1
  1. 1.Department of Biology and Museum of Southwestern BiologyUniversity of New MexicoAlbuquerqueUSA
  2. 2.Pronatura Noreste, A. C.MonterreyMéxico
  3. 3.Laboratorio de Ictiología, Facultad de Ciencias BiológicasUniversidad Autónoma de Nuevo LeónSan Nicolás de los GarzaMéxico

Personalised recommendations