Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2019-07-23
Page range: 145–163
Abstract views: 172
PDF downloaded: 1

Genetic and phenotypic diversity of Branchinecta sandiegonensis (Crustacea: Anostraca) in the vernal pools of Baja California, México

1Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE). Ensenada, Baja California, México.
Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE). Ensenada, Baja California, México.
Departamento de Biología de la Conservación, Centro de Investigación Científica y de Educación Superior de Ensenada (CICESE). Ensenada, Baja California, México.
Facultad de Ciencias, Universidad Autónoma de Baja California. Ensenada, Baja California, México.
Department of Conservation and Research, Santa Barbara Botanic Garden. Santa Barbara, California, the United States of America.
Crustacea Demography Mediterranean-type climate region population genetics morphometric variation fairy shrimp

Abstract

Branchinecta sandiegonensis is a passively dispersed species that occurs in the vernal pool complexes of southern California, the USA, and northwestern Baja California, México. The fragmented distribution of these vernal pool complexes could limit the gene flow, generating high genetic structure and morphometric variation across the landscape. Here we estimate the genetic and phenotypic variation of B. sandiegonensis in the southern part of its range. We sampled 15 vernal pools from four geographic regions of the Baja California Peninsula. We genotyped 150 individuals using nuclear microsatellites and 31 individuals using the mitochondrial COI region. We also conducted a morphometric analysis on a sample of 232 individuals. We found moderate levels of genetic diversity and different patterns of structure depending upon the spatial scale of analysis. Demographic models suggest contrasting trends among populations. Phenotypically, we found high levels of heterogeneity in body size of fairy shrimps within and across the regions. Our findings highlight that vernal pools in Baja California are important reservoirs of genetic and phenotypic diversity for B. sandiegonensis. The interplay between gene flow and genetic drift may have influenced the patterns we detected in the southern part of the range of this species.

 

References

  1. Adamack, A.T. & Gruber, B. (2014) PopGenReport: simplifying basic population genetic analyses in R. Methods in Ecology and Evolution, 5 (4), 384–387.

    https://doi.org/10.1111/2041-210X.12158

    Aguilar, A., Maeda-Martínez, A.M., Murugan, G., Obregón-Barboza, H., Rogers, D.C., McClintock, K. & Krumm, J.L. (2017) High intraspecific genetic divergence in the versatile fairy shrimp Branchinecta lindahli with a comment on cryptic species in the genus Branchinecta (Crustacea: Anostraca). Hydrobiologia, 801 (1), 59–69.

    https://doi.org/10.1007/s10750-017-3283-3

    Andrews, J.M. (2013) Conservation genetics of the endangered San Diego fairy shrimp (Branchinecta sandiegonensis). San Diego State University, San Diego, California, 81 pp.

    Andrews, J.M., Bohonak, A.J. & Simovich, M.A. (2014) Isolation and characterization of polymorphic microsatellite loci in the endangered San Diego fairy shrimp (Branchinecta sandiegonensis). Conservation Genetics Resources, 6 (2), 401–403.

    https://doi.org/10.1007/s12686-013-0103-6

    Atashbar, B., Agh, N., Manaffar, R., Stappen, G.V., Mohamadyari, A., Mertens, J. & Beladjal, L. (2016) Morphometric and preliminary genetic characteristics of Branchinecta orientalis populations from Iran (Crustacea: Anostraca). Zootaxa, 4109 (1), 31–45.

    https://doi.org/10.11646/zootaxa.4109.1.3

    Bohonak, A.J. (1998) Genetic population structure of the fairy shrimp Branchinecta coloradensis (Anostraca) in the Rocky Mountains of Colorado. Canadian Journal of Zoology, 76 (11), 2049–2057.

    https://doi.org/10.1139/z98-170

    Bohonak, A.J. & Jenkins, D.G. (2003) Ecological and evolutionary significance of dispersal by freshwater invertebrates. Ecology letters, 6 (8), 783–796.

    https://doi.org/10.1046/j.1461-0248.2003.00486.x

    Bohonak, A.J. (2005) MSCP vernal pool inventory City of San Diego (USFWS) Conservation genetics of the endangered fairy shrimp species Branchinecta sandiegonensis. Available from: https://sdmmp.com/upload/SDMMP_Repository/0/b2tmn34dzwrysx1q6pfj89g0k75.pdf (accessed 12 April 2014)

    Boileau, M.G., Hebert, P.D. & Schwartz, S.S. (1992) Non-equilibrium gene frequency divergence: persistent founder effects in natural populations. Journal of Evolutionary Biology, 5 (1), 25–39.

    https://doi.org/10.1046/j.1420-9101.1992.5010025.x

    Boix, D., Kneitel, J., Robson, B.J., Duchet, C., Zúñiga, L., Day, J., Gascón, S., Sala, J., Quintana, X.D. & Blaustein, L. (2016) Invertebrates of freshwater temporary ponds in Mediterranean climates. In: Batzer, D. & Boix, D. (Eds.), Invertebrates in Freshwater Wetlands. Springer, Cham, pp. 141–189.

    https://doi.org/10.1007/978-3-319-24978-0_5

    Brendonck, L., De Meester, L. & Riddoch, B.J. (2000) Regional structuring of genetic variation in short-lived rock pool populations of Branchipodopsis wolfi (Crustacea: Anostraca). Oecologia, 123 (4), 506–515.

    https://doi.org/10.1007/s004420000344

    Brendonck, L., Rogers, D.C., Olesen, J., Weeks, S. & Hoeh, W.R. (2008) Global diversity of large branchiopods (Crustacea: Branchiopoda) in freshwater. Hydrobiologia, 595 (1), 167–176.

    https://doi.org/10.1007/s10750-007-9119-9

    Chapuis, M.P. & Estoup, A. (2007) Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution, 24 (3), 621–631.

    https://doi.org/10.1093/molbev/msl191

    Cohen, R.G. (2012) Morphological diversity displayed by high altitude Branchinecta papillata (Anostraca) and additional morphological comparisons with Branchinecta achalensis. Journal of Crustacean Biology, 32 (1), 1–13.

    https://doi.org/10.1163/193724011X617404.

    Davies, C.P., Simovich, M.A. & Hathaway, S.A. (1997) Population genetic structure of a California endemic branchiopod, Branchinecta sandiegonensis. In: Simovich, M.A., Sassaman, C. & Belk, D. (Eds.), Developments in Hydrobiology. Vol. 125. Studies on Large Branchiopod Biology and Conservation. Springer Dordrecht, pp. 149–158.

    https://doi.org/10.1007/978-94-017-3177-5_15

    Deiner, K., Hull, J.M. & May, B. (2017) Range-wide phylogeographic structure of the vernal pool fairy shrimp (Branchinecta lynchi). PloS one, 12 (5), e0176266.

    https://doi.org/10.1371/journal.pone.0176266

    De Meester, L., Gómez, A., Okamura, B. & Schwenk, K. (2002) The Monopolization Hypothesis and the dispersal–gene flow paradox in aquatic organisms. Acta oecologica, 23 (3), 121–135.

    https://doi.org/10.1016/S1146-609X(02)01145-1

    Di Rienzo, A., Peterson, A.C., Garza, J.C., Valdes, A.M., Slatkin, M. & Freimer, N.B. (1994) Mutational processes of simple-sequence repeat loci in human populations. Proceedings of the National Academy of Sciences of the United States of America, 91 (8), 3166–3170.

    https://doi.org/10.1073/pnas.91.8.3166

    Dzialowski, A.R., Lennon, J.T., O’Brien, W.J. & Smith, V.H. (2003) Predator-induced phenotypic plasticity in the exotic cladoceran Daphnia lumholtzi. Freshwater Biology, 48 (9), 1593–1602.

    https://doi.org/10.1046/j.1365-2427.2003.01111.x.

    Earl, D.A. & Vonholdt, B.M. (2012) Structure Harvester: a website and program for visualizing Structure output and implementing the Evanno method. Conservation Genetics Resources, Series 4, 359–361.

    https://doi.org/10.1007/s12686-011-9548-7

    Edwards, A.W.F. (1971) Distance between populations on the basis of gene frequencies. Biometrics, 27 (4), 873–881.

    https://doi.org/10.2307/2528824

    Eriksen, C.H. & Belk, D. (1999) Fairy shrimps of California’s puddles, pools, and playas. Mad River Press, Eureka California, xiv + 196 pp.

    Evanno, G., Regnault, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software STRUCTURE: A simulation study. Molecular Ecology, 14, 2611–2620.

    https://doi.org/10.1111/j.1365-294X.2005.02553.x

    Falush, D., Stephens, M. & Pritchard, J.K. (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics, 164 (4), 1567–1587.

    Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology, 3 (5), 294–9.

    Forsman, A. (2014) Effects of genotypic and phenotypic variation on establishment are important for conservation, invasion, and infection biology. Proceedings of the National Academy of Sciences of the United States of America, 111 (1), 302–307. https://doi.org/10.1073/pnas.1317745111

    Frankham, R. (2008) Inbreeding and extinction: island populations. Conservation biology, 12(3), 665–675.

    https://doi.org/10.1111/j.1523-1739.1998.96456.x

    Fugate, M.L. (1993) Branchinecta sandiegonensis, a new species of fairy shrimp (Crustacea: Anostroca) from Western North America. Proceedings of the Biological Society of Washington, 106 (2), 296–304.

    Gerlach, G., Jueterbock, A., Kraemer, P., Deppermann, J. & Harmand, P. (2010) Calculations of population differentiation based on GST and D: forget GST but not all of statistics! Molecular Ecology, 19 (18), 3845–3852.

    https://doi.org/10.1111/j.1365-294X.2010.04784.x

    Goddard, N.S. (2017) Landscape Genetics of the Endangered San Diego Fairy Shrimp (Branchinecta sandiegonensis). San Diego State University, San Diego, California, 60 pp.

    Goudet, J. & Jombart, T. (2015) hierfstat: Estimation and Tests of Hierarchical F Statistics. R package. Version 0.04-22. Available from: https://cran.r-project.org/web/packages/hierfstat/index.html(accessed 4 April 2016)

    Guilliams, C.M., Hasenstab-Lehman, K., Delgadillo, J. & Baldwin, B.G. (2016) Vernal pool landscapes of Baja California, México: An ongoing project to assess vernal pool loss and to protect what remains. In: Schlising, R.A., Gottschalk-Fisher, E.E. & Guilliams, C.M. (Eds.), Vernal pools in changing landscapes. Number 18. Studies from the herbarium, California State University, Chico, California, pp. 263–291.

    Hathaway, S.A. & Simovich, M.A. (1996) Factors affecting the distribution and co-occurrence of two southern Californian anostracans (Branchiopoda), Branchinecta sandiegonensis and Streptocephalus woottoni. Journal of Crustacean Biology, 16 (4), 669–677.

    https://doi.org/10.1163/193724096X00757.

    Hedrick, P.W. (2005) Genetics of populations. Jones and Bartlett Publishers, Sudbury Massachusetts, 737 pp.

    Hijmans, R.J., Van Etten, J. & Cheng, J. (2016) Package raster. R Foundation for Statistical Computing. Available from: https://cran.r-project.org/package=raster (accessed 12 September 2017)

    Hulsmans, A., Moreau, K., De Meester, L., Riddoch, B.J. & Brendonck, L. (2007) Direct and indirect measures of dispersal in the fairy shrimp Branchipodopsis wolfi indicate a small scale isolation-by-distance pattern. Limnology and Oceanography, 52 (2), 676–684.

    https://doi.org/10.4319/lo.2007.52.2.0676

    Incagnone, G., Marrone, F., Barone, R., Robba, L. & Naselli-Flores, L. (2015) How do freshwater organisms cross the “dry ocean? A review on passive dispersal and colonization processes with a special focus on temporary ponds. Hydrobiologia, 750 (1), 103–123.

    https://doi.org/10.1007/s10750-014-2110-3

    INEGI. (2014) Información por entidad: Baja California. Available from: http://cuentame.inegi.org.mx/monografias/informacion/bc/territorio/clima.aspx?tema=me&e=02 (accessed 15 September 2015)

    Jombart, T. & Ahmed, I. (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics, 27 (21), 3070–3071.

    https://doi.org/10.1093/bioinformatics/btr521

    Jost, L. (2008) Gst and its relatives do not measure differentiation. Molecular Ecology, 17 (18), 4015–4026.

    https://doi.org/10.1111/j.1365-294X.2008.03887.x

    Kamvar, Z.N., Tabima, J.F. & Grünwald, N.J. (2014) Poppr: an R package for genetic analysis of populations with clonal, partially clonal, and/or sexual reproduction. PeerJ, 2, e281.

    https://doi.org/10.7717/peerj.281

    Keeley, J.E. & Zedler, P.H. (1998) Characterization and global distribution of vernal pools. In: Witham, C.W., Bauder, E.T., Belk, D., Ferren Jr., W.R. & Ornduff, R. (Eds.), Ecology, conservation, and management of vernal pool ecosystems: proceedings from a 1996 conference. California Native Plant Society, Sacramento, CA, pp. 1–14.

    Keyghobadi, N. (2007) The genetic implications of habitat fragmentation for animals. Canadian Journal of Zoology, 85 (10), 1049–1064.

    https://doi.org/10.1139/Z07-095

    Lande, R. & Shannon, S. (1996) The role of genetic variation in adaptation and population persistence in a changing environment. Evolution, 50 (1), 434–437.

    https://doi.org/10.2307/2410812

    Leray, M., Yang, J.Y., Meyer, C.P., Mills, S.C., Agudelo, N., Ranwez, V., Boehm, J. & Machida, R.J. (2013) A new versatile primer set targeting a short fragment of the mitochondrial COI region for metabarcoding metazoan diversity: application for characterizing coral reef fish gut contents. Frontiers in Zoology, 10 (1), 34.

    https://doi.org/10.1186/1742-9994-10-34

    Librado, P. & Rozas, J. (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics, 25 (11), 1451–1452.

    https://doi.org/10.1093/bioinformatics/btp187

    Mantel, N.A. (1967) The detection of disease clustering and a generalized regression approach. Cancer Research, 27 (2), 209–220.

    Martijena, N.E. (2003) El Niño-Southern Oscillation and precipitation history in Baja California: reconstruction using tree ring records. Geofísica Internacional, 42 (3), 351–362.

    Meko, D.M., Stockton, C.W. & Boggess, W.R. (1980) A tree-ring reconstruction of drought in southern California. Journal of the American Water Resources Association, 16 (4), 594–600.

    https://doi.org/10.1111/j.1752-1688.1980.tb02436.x

    Monmonier, M.S. (1973) Maximum-difference barriers: an alternative numerical regionalization method. Geographical Analysis, 5 (3), 245–261.

    https://doi.org/10.1111/j.1538-4632.1973.tb01011.x

    Montiel, J.A. (2013) Distribución de flora endémica y rara de charcas vernales en relación a las propiedades fisicoquímicas del suelo. Centro de Investigación Científica y de Educación Superior de Ensenada, Baja California (CISESE), México, 68 pp.

    Nikolic, N. & Chevalet, C. (2014) Detecting past changes of effective population size. Evolutionary Applications, 7 (6), 663–681.

    https://doi.org/10.1111/eva.12170

    Obregón-Barboza, H., Murugan, G., García-Velazco, H. & Maeda-Martínez, A.M. (2015) A review of the Branchinecta (Branchiopoda: Anostraca) from the Baja California Peninsula: first record of the giant fairy shrimp B. gigas Lynch, 1937 from México. Journal of Crustacean Biology, 35 (3), 433–440.

    https://doi.org/10.1163/1937240X-00002321

    Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25 (7), 1253–1256.

    https://doi.org/10.1093/molbev/msn083

    Pritchard, J.K., Stephens, M. & Donnelly, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155 (2), 945–959.

    Rambaut, A., Drummond, A.J., Xie, D., Baele, G. & Suchard, M.A. (2018) Posterior summarisation in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67 (5), 901–904.

    https://doi.org/10.1093/sysbio/syy032

    R Core Team. (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. Available from: https://www.R-project.org/ (accessed 15 August 2017)

    Rogers, D.C. (2013) Anostraca Catalogus (Crustacea: Branchiopoda). The Raffles Bulletin of Zoology, 61 (2), 525–546.

    Rogers, D.C. (2015) A conceptual model for Anostracan biogeography. Journal of Crustacean Biology, 35 (5), 686–699.

    https://doi.org/10.1163/1937240X-00002369

    Rosete Vergés, F.A., Velázquez, A., Bocco, G. & Espejel, I. (2014) Multi-scale land cover dynamics of semiarid scrubland in Baja California, México. Regional environmental change, 14 (4), 1315–1328.

    https://doi.org/10.1007/s10113-013-0574-8

    Rousset, F. (2008) Genepop’007: a complete re-implementation of the Genepop software for Windows and Linux. Molecular Ecology Resources, 8 (1), 103–106.

    https://doi.org/10.1111/j.1471-8286.2007.01931.x

    Simovich, M.A., Davis, K.B. & Bohonak, A.J. (2013) Landscape homogenization threatens the genetic integrity of the endangered San Diego fairy shrimp Branchinecta sandiegonensis (Branchiopoda: Anostraca). Journal of Crustacean Biology, 33 (5), 730–740. https://doi.org/10.1163/1937240X-00002164

    Simovich, M.A. & Hathaway, S.A. (1997) Diversified bet-hedging as a reproductive strategy of some ephemeral pool anostracans (Branchiopoda). Journal of Crustacean Biology, 17 (1), 38–44.

    https://doi.org/10.1163/193724097X00070

    Slatkin, M. (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution, 47 (1), 264–279.

    https://doi.org/10.2307/2410134

    Suchard, M.A., Lemey, P., Baele, G., Ayres, D.L., Drummond, A.J. & Rambaut, A. (2018) Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution, 4 (1), vey016.

    https://doi.org/10.1093/ve/vey016

    Steele, A.N., Simovich, M.A., Pepino, D., Schroeder, K.M., Vandergast, A.G. & Bohonak, A.J. (2009) Optimized DNA extraction methods for encysted embryos of the endangered fairy shrimp, Branchinecta sandiegonensis. Conservation genetics, 10 (6), 1777.

    https://doi.org/10.1007/s10592-008-9733-8

    Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution, 30 (12), 2725–2729.

    https://doi.org/10.1093/molbev/mst197

    Thompson, J.N. (2005) The geographic mosaic of coevolution. University of Chicago Press, Chicago, Illinois, 400 pp.

    https://doi.org/10.7208/chicago/9780226118697.001.0001

    Van Oosterhout, C., Hutchinson, W.F., Wills, D.P.M. & Shipley, P. (2004) Micro-checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Resources, 4 (3), 535–538.

    https://doi.org/10.1111/j.1471-8286.2004.00684.x

    Vandergast, A.G., Wood, D.A., Simovich, M. & Bohonak, A.J. (2009) Identification of co-occurring Branchinecta fairy shrimp species from encysted embryos using multiplex polymerase chain reaction. Molecular Ecology Resources, 9 (3), 767–770.

    https://doi.org/10.1111/j.1755-0998.2009.02522.x

    Ward Jr., J.H. (1963) Hierarchical grouping to optimize an objective function. Journal of the American Statistical Association, 58 (301), 236–244.

    https://doi.org/10.1080/01621459.1963.10500845

    Waples, R.S. & Gaggiotti, O. (2006). What is a population? An empirical evaluation of some genetic methods for identifying the number of gene pools and their degree of connectivity. Molecular Ecology, 15 (6), 1419–1439.

    Weir, B.S. & Cockerham, C.C. (1984) Estimating F-statistics for the analysis of population structure. Evolution, 38 (6), 1358–1370.

    https://doi.org/10.2307/2408641

    Wright, S. (1965) The interpretation of population structure by F-statistics with special regard to systems of mating. Evolution, 19 (3), 395–420.

    https://doi.org/10.1111/j.1558-5646.1965.tb01731.x

    Zickovich, J.M. & Bohonak, A.J. (2007) Dispersal ability and genetic structure in aquatic invertebrates: a comparative study in southern California streams and reservoirs. Freshwater Biology, 52 (10), 1982–1996.

    https://doi.org/10.1111/j.1365-2427.2007.01822.x

    Zofkova, M. & Timms, B.V. (2009) A conflict of morphological and genetic patterns in the Australian anostracan Branchinella longirostris. Hydrobiologia, 635 (1), 67–80.

    https://doi.org/10.1007/s10750-009-9862-1