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Hydrobiologia

, Volume 801, Issue 1, pp 59–69 | Cite as

High intraspecific genetic divergence in the versatile fairy shrimp Branchinecta lindahli with a comment on cryptic species in the genus Branchinecta (Crustacea: Anostraca)

  • Andres Aguilar
  • Alejandro M. Maeda-Martínez
  • Gopal Murugan
  • Hortencia Obregón-Barboza
  • D. Christopher Rogers
  • Kelly McClintock
  • Janice L. Krumm
CHALLENGES IN ANOSTRACAN RESEARCH

Abstract

Branchinecta lindahli is a generalist fairy shrimp that has a widespread distribution in North America. We initiated a study to better understand the geographic structure of genetic variation within this species and to test if cryptic species are present in B. lindahli. Additionally, we examined four other species of Branchinecta to test if there were any generalities in the levels of genetic divergence within and among species. Genetic data from the mitochondrial cytochrome c oxidase I gene revealed two distinct clades within B. lindahli: one found in the Central Valley and Mojave Desert of California, USA and one found in Baja California, Mexico. The remaining haplotypes were widespread throughout the remainder of North America. Further examination of the distribution within clades revealed no additional phylogeographic structure. The amount of intraspecific divergence observed for B. lindahli and B. hiberna was high compared to B. mackini and B. sandiegonensis. However, maximal intraspecific divergences were less than what was observed among Branchinecta species. We argue that the amount of intraspecific divergence observed in B. lindahli is not consistent with the presence of cryptic species and that caution should be taken when attempting to delimit cryptic species within this group.

Keywords

Branchinectidae Cytochrome oxidase I North America Phylogeography 

Notes

Acknowledgements

We thank Mr. Humberto García-Velazco and Mr. José Ángel Camacho for helping during field collection in Baja California, Mexico. Mr. J. Lopez and Mr. J. Ulloa assisted in the generation of genetic data. This study was supported by a grant from the UC MEXUS-CONACYT program to AA and AMMM (Project No. CN08). Collections made by AA and AMMM were done so under scientific collecting permits SCP-17338 (CDFW) and SGPA/DGVS/08331/10, respectively. We also thank Dr. M. Schwentner and two anonymous reviewers for comments on an earlier version of this manuscript.

Supplementary material

10750_2017_3283_MOESM1_ESM.xlsx (10 kb)
Supplementary material 1 (XLSX 10 kb)

References

  1. Aguilar, A., 2011. Weak phylogeographic structure in the endemic western North American fairy shrimp Branchinecta lynchi (Eng, Belk and Eriksen 1990). Aquatic Sciences 73: 15–20.CrossRefGoogle Scholar
  2. Bandelt, H. J., P. Forster & A. Röhl, 1999. Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16: 37–48.CrossRefPubMedGoogle Scholar
  3. Belk, D., 1975. Key to the Anostraca (fairy shrimps) of North America. The Southwestern Naturalist 20: 91–103.CrossRefGoogle Scholar
  4. Belk, D., 1977. Zoogeography of the Arizona fairy shrimps (Crustacea: Anostraca). Arizona Academy of Sciences 12: 70–78.CrossRefGoogle Scholar
  5. Belk, D., 1983. New fairy shrimp distribution records among collections at the California Academy of Sciences. The Southwestern Naturalist 28: 380–381.CrossRefGoogle Scholar
  6. Belk, D. & J. Brtek, 1995. Checklist of the Anostraca. Hydrobiologia 298: 315–353.CrossRefGoogle Scholar
  7. Belk, D. & J. Brtek, 1997. Supplement to ‘Checklist of the Anostraca’. Hydrobiologia 359: 243–245.CrossRefGoogle Scholar
  8. Belk, D. & D. R. Lindberg, 1979. First freshwater animal reported for Isla de Guadalupe represents a southern range extension for Branchinecta lindahli. (Crustacea: Anostraca). The Southwestern Naturalist 24: 390–391.CrossRefGoogle Scholar
  9. Bohonak, A. & D. Jenkins, 2003. Ecological and evolutionary significant of dispersal by freshwater invertebrates. Ecology Letters 6: 783–796.CrossRefGoogle Scholar
  10. Boileau, M. G., P. N. D. Hebert & S. S. Schwartz, 1992. Nonequilibrium gene frequency divergence – persistent founder effects in natural populations. Journal of Evolutionary Biology 5: 25–39.CrossRefGoogle Scholar
  11. Costa, F. O., J. R. de Waard, J. Boutillier, S. Ratnasingham, R. T. Dooh, M. Hajibabae & P. D. N. Hebert, 2007. Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64: 272–295.CrossRefGoogle Scholar
  12. De Gelas, K. & L. De Meester, 2005. Phylogeography of Daphnia magna in Europe. Molecular Ecology 14: 753–763.CrossRefPubMedGoogle Scholar
  13. De Meester, L., A. Gomez, B. Okamura & K. Schwenk, 2002. The monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms. Acta Oecologia 23: 121–135.CrossRefGoogle Scholar
  14. Dexter, R. W., 1956. A new fairy shrimp from western United States, with notes on other North American species. Journal of the Washington Academy of Sciences 46: 159–165.Google Scholar
  15. Eng, L. L., D. Belk & C. H. Eriksen, 1990. Californian Anostraca: Distribution, habitat, and status. Journal of Crustacean Biology 10: 247–277.CrossRefGoogle Scholar
  16. Eriksen, C. H. & D. Belk, 1999. The fairy shrimps of California’s pools, puddles, and playas. Mad River Press, Eureka: 196.Google Scholar
  17. Folmer, O., M. Black, W. Hoeh, R. Lutz & R. Vrijenhoek, 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3: 294–299.PubMedGoogle Scholar
  18. Fugate, M., 1993. Branchinecta sandiegonensis, a new species of fairy shrimp (Crustacea: Anostraca) from western North America. Proceedings of the Biological Society of Washington 106: 296–304.Google Scholar
  19. Gomez, A., J. Montero-Pau, D. H. Lunt, M. Serra & S. Campillo, 2007. Persistent genetic signatures of colonization in Branchionus manjavacas rotifers in the Iberian Peninsula. Molecular Ecology 16: 3228–3240.CrossRefPubMedGoogle Scholar
  20. Hartland-Rowe, R., 1965. The Anostraca and Notostraca of Canada with some new distribution records. The Canadian Field Naturalist 79: 185–189.Google Scholar
  21. Hebert, P. D. N., J. D. S. Witt & S. J. Adamowicz, 2003. Phylogeographical patterning in Daphnia ambigua: Regional divergence and intercontinental cohesion. Limnology and Oceanography 48: 261–268.CrossRefGoogle Scholar
  22. Hebert, P. D., M. Y. Stoeckle, T. S. Zemlak & C. M. Francis, 2004. Identification of birds through DNA barcodes. PLoS Biology 2: e312.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Horne, F. R., 1967. Effects of physical-chemical factors on the distribution and occurrence of some southeastern Wyoming phyllopods. Ecology 48: 472–477.CrossRefGoogle Scholar
  24. Horne, F. R., 1971. Some effects of temperature and oxygen concentration on phyllopod ecology. Ecology 52: 343–347.CrossRefGoogle Scholar
  25. Ketmaier, V., R. Mandatori, E. DeMatthaeis & G. Mura, 2005. Molecular systematics and phylogeography in the fairy shrimp Tanymastix stagnalis based on mitochondrial DNA. Journal of Zoology 206: 401–410.CrossRefGoogle Scholar
  26. Ketmaier, V., F. Marrone, G. Alfonso, K. Paulus, A. Wiemann, R. Tiedemann & G. Mura, 2012. Mitochondrial DNA regionalism and historical demography in the extant populations of Chirocephalus kerkyrensis (Branchiopoda: Anostraca). PLoS ONE 7: e30082.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lefébure, T., C. J. Douady, M. Gouy & J. Gibert, 2006. Relationship between morphological taxonomy and molecular divergence within Crustacea: proposal of a molecular threshold to help species delimitation. Molecular Phylogenetics and Evolution 40: 435–447.CrossRefPubMedGoogle Scholar
  28. Leigh, J. W. & D. Bryant, 2015. POPART: full-feature software for haplotype network construction. Methods in Ecology and Evolution 6: 1110–1116.CrossRefGoogle Scholar
  29. Librado, P. & J. Rozas, 2009. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452.CrossRefPubMedGoogle Scholar
  30. Lindholm, M., M. A. D’auriac, J. Thaulow & A. Hobæk, 2016. Dancing around the pole: Holarctic phylogeography of the Arctic fairy shrimp Branchinecta paludosa (Anostraca, Branchiopoda). Hydrobiologia 772: 189–205.CrossRefGoogle Scholar
  31. Lynch, J. E., 1964. Packard’s and Pearse’s species of Branchinecta: Analysis of a nomenclatural involvement. Amercan Midland Naturalist 71: 466–488.CrossRefGoogle Scholar
  32. Maeda-Martínez, A. M., 1991. Distribution of species of Anostraca, Notostraca, Spinicaudata, and Laevicaudata in Mexico. Hydrobiologia 212: 209–212.CrossRefGoogle Scholar
  33. Maeda-Martínez, A. M., H. Obregón-Barboza & H. García-Velazco, 1997. New records of large branchiopods (Branchiopoda: Anostraca, Notostraca, and Spinicaudata) in Mexico. Hydrobiologia 359: 63–68.CrossRefGoogle Scholar
  34. Maeda-Martínez, A. M., H. Obregon-Barboza, H. García-Velazco, & M. A. Prieto-Salazar. 2002. Branchiopoda: Anostraca, In: Bousquets, J. L., and J. J. Morrone (eds) Biodiversidad, Taxonomía y Biogeografía de Artrópodos de México: hacia una síntesis de su conocimiento, Vol. III. Universidad Nacional Autonóma de México, pp. 305–322.Google Scholar
  35. Millette, K. L., S. Xu, J. D. Witt & M. E. Cristescu, 2011. Pleistocene-driven diversification in freshwater zooplankton: Genetic patterns of refugial isolation and postglacial recolonization in Leptodora kindtii (Crustacea, Cladocera). Limnology and Oceanography 56: 1725–1736.CrossRefGoogle Scholar
  36. Meusel, F. & M. Schwentner, 2016. Molecular and morphological delimitation of Australian Triops species (Crustacea: Branchiopoda: Notostraca)—large diversity and little morphological differentiation. Organisms Diversity & Evolution 17: 1–20.Google Scholar
  37. Muñoz, J., A. Gomez, A. J. Green, J. Figuerola, F. Amat & C. Rico, 2008. Phylogeography and local endemism of the native Mediterranean brine shrimp Artemia salina (Branchiopoda: Anostraca). Molecular Ecology 17: 3160–3177.CrossRefPubMedGoogle Scholar
  38. Obregón-Barboza, H., A. M. Maeda-Martínez, H. García-Velazco & H. J. Dumont, 2002. Branchinecta oterosanvicentei n. sp. (Branchiopoda: Anostraca), a new fairy shrimp from the Chihuahuan desert, with a proposal for the conservation of the Branchinectidae of Mexico. Hydrobiologia 467: 45–56.CrossRefGoogle Scholar
  39. Obregón-Barboza, H., G. Murugan, H. García-Velazco & A. M. Maeda-Martínez, 2015a. A systematic review of mexican populations of the fairy shrimp genus Thamnocephalus (Branchiopoda: Anostraca). Journal of Crustacean Biology 35: 407–432.CrossRefGoogle Scholar
  40. Obregón-Barboza, H., G. Murugan, H. García-Velazco & A. M. Maeda-Martínez, 2015b. A review of the Branchinecta (Branchiopoda: Anostraca) from the Baja California Peninsula: First record of the giant fairy shrimp B. gigas Lynch, 1937 from Mexico. Journal of Crustacean Biology 35: 433–440.CrossRefGoogle Scholar
  41. Packard, A. S., 1877. Description of new phyllopod Crustacea from the West. Bulletin of the United States Geological and Geographical Survey of the Territories 3: 171–179.Google Scholar
  42. Packard, A. S., 1883. A monograph of the phyllopod Crustacea of North America, with remarks on the order Phyllocarida. Twelfth annual report of the United States Geological and Geographical Survey of the Territories: a report of progress of the exploration in Wyoming and Idaho for the year 1878, F. V. Hayden, Part 1, section 2: 295–593.Google Scholar
  43. Penton, E. H., P. D. Hebert & T. J. Crease, 2004. Mitochondrial DNA variation in North American populations of Daphnia obtusa: continentalism or cryptic endemism? Molecular Ecology 13: 97–107.CrossRefPubMedGoogle Scholar
  44. Posada, D., 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25: 1253–1256.CrossRefPubMedGoogle Scholar
  45. Rogers, D. C. 2009. Branchiopoda (Anostraca, Notostraca, Laevicaudata, Spinicaudata, Cyclestherida). In: Likens, G. F. (editor) Encyclopedia of Inland Waters, vol. 2, pp. 242–249.Google Scholar
  46. Rogers, D. C., 2013. Anostraca catalogus (Crustacea: Branchiopoda). The Raffles Bulletin of Zoology. 61: 525–546.Google Scholar
  47. Rogers, D. C. & M. A. Hill, 2013. Annotated Checklist of the large branchiopod crustaceans of Idaho, Oregon and Washington, USA, with the “rediscovery” of a new species of Branchinecta (Anostraca: Branchinectidae). Zootaxa 3694: 249–261.Google Scholar
  48. Rogers, D. C., 2014a. Anostracan (Crustacea: Branchiopoda) zoogeography II. Relating distribution to geochemical substrate properties in the USA. Zootaxa 3865: 1–49.CrossRefGoogle Scholar
  49. Rogers, D. C., 2014b. Larger hatching fractions in avian dispersed anostracan eggs (Branchiopoda). Journal of Crustacean Biology 34: 135–143.CrossRefGoogle Scholar
  50. Rogers, D. C., 2015. A conceptual model for anostracan biogeography. Journal of Crustacean Biology 35: 686–699.CrossRefGoogle Scholar
  51. Rogers, D. C. & M. Fugate, 2001. Branchinecta hiberna, a new species of fairy shrimp (Crustacea: Anostraca) from western North America. Western North American Naturalist 61: 11–18.Google Scholar
  52. Rogers, D. C., D. Quinney, J. Weaver & J. Olesen, 2006. A new giant species of predatory fairy shrimp from Idaho (Branchiopoda: Anostraca). Journal of Crustacean Biology 26: 1–16.CrossRefGoogle Scholar
  53. Ronquist, F. & J. P. Huelsenbeck, 2003. MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572–1574.CrossRefPubMedGoogle Scholar
  54. Ryder, J. A., 1879. Description of a new branchiopod. Proceedings of the Academy of Natural Sciences of Philadelphia 1879: 200–202.Google Scholar
  55. Schwentner, M., B. V. Timms & S. Richter, 2011. An integrative approach to species delineation incorporating different species concepts: a case study of Limnadopsis (Branchiopoda: Spinicaudata). Biological Journal of the Linnean Society 104: 575–599.CrossRefGoogle Scholar
  56. Schwentner, M., B. V. Timms & S. Richter, 2014. Evolutionary systematics of the Australian Eocyzicus fauna (Crustacea: Branchiopoda: Spinicaudata) reveals hidden diversity and phylogeographic structure. Journal of Zoological Systematics and Evolutionary Research 52: 15–31.CrossRefGoogle Scholar
  57. Schwentner, M., B. V. Timms & S. Richter, 2015. Spinicaudata (Branchiopoda: Diplostraca) in Australia’s arid zone: unparalleled diversity at regional scales and within water bodies. Journal of Crustacean Biology 35: 366–378.CrossRefGoogle Scholar
  58. Tamura, K., J. Dudley, M. Nei & S. Kumar, 2007. MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.CrossRefPubMedGoogle Scholar
  59. Vandergast, A. G., D. A. Wood, M. A. Simovich & A. J. Bohonak, 2009. Identification of co-occurring Branchinecta fairy shrimp species from encysted embryos using multiplex polymerase chain reaction. Molecular Ecology Resources 9: 767–770.CrossRefPubMedGoogle Scholar
  60. Xu, S., P. D. N. Hebert, A. A. Kotov & M. E. Cristescu, 2009. The noncosmopolitanism paradigm of freshwater zooplankton: insights from the global phylogeography of the predatory cladoceran Polyphemus pediculus (Linnaeus, 1761) (Crustacea, Onychopoda). Molecular Ecology 18: 5161–5179.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.School of Natural Sciences and Sierra Nevada Research InstituteUniversity of CaliforniaMercedUSA
  2. 2.Department of Biological SciencesCalifornia State University, Los AngelesLos AngelesUSA
  3. 3.Centro de Investigaciones Biológicas del Noroeste (CIBNOR), Calle Instituto Politécnico Nacional 195La PazMexico
  4. 4.Kansas Biological SurveyUniversity of KansasLawrenceUSA
  5. 5.Department of BiologyWidener UniversityChesterUSA

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