Skip to main content

Islands in the desert: assessing fine scale population genomic variation of a group of imperiled desert fishes

Abstract

The genus Crenichthys (Teleostei: Goodeidae) is an imperiled group of desert spring specialist fishes currently containing two species and five subspecies, found within only a few of the relictual springs distributed throughout the Great Basin of North America. Threatened by multiple forms of human disturbance, including habitat destruction, invasive species, and pollution, the need to better understand their population structure is immediate. This is further emphasized by previous research that demonstrated that the current taxonomy of Crenichthys needs re-evaluation and that genetic substructure may be present. The genus also represents a perfect opportunity to better understand desert spring habitats. These unique ecosystems often contain a suite of endemics, trapped within individual isolated springs distributed throughout a desert. The assumption is often that each spring will contain genetically distinct populations, however, this is not always true. We used single nucleotide polymorphisms (SNPs) to describe the genetic diversity and structure among populations of the genus Crenichthys with the intent to better understand the patterns of diversity within desert endemic fishes. Our results corroborated previous research suggesting genetic divergence between two groups within both C. baileyi and C. nevadae. It further demonstrated that many of the populations are genetically similar, likely due to a combination of short divergence time and possible past admixture.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Data Availability, material, and code

The data and datasets generated/analyzed during the current study are available on DataDryad (https://doi.org/10.5061/dryad.prr4xgxpc).

References

  • Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19:1655–1664

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Axelrod DI (1979) Age and origin of Sonoran Desert vegetation. Occ Pap California Acad Sci 132:1–74

    Google Scholar 

  • Baird N, Etter PD, Atwood TS et al (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS ONE 3:1–7

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B Methodological 57:289–300

    Google Scholar 

  • Caldu-Primo J, Mastretta-Yanes A, Wegier A, Pinero D (2017) Finding a needle in a haystack: Distinguishing Mexican maze landraces using a small number of SNPs. Front Genet 8:1–12

    Article  Google Scholar 

  • Campbell DC, Piller KR (2017) Let’s jump in: A phylogeographic study of the Great Basin springfish and poolfishes, Crenichthys and Empetrichthys (Cyprinodontiformes: Goodeinae). PLoS ONE 12:1–21

  • Corander J, Majander KK, Cheng L, Merila J (2013) High degree of cryptic population differentiation in the Baltic Sea herring Clupea harengus. Mol Ecol 22:2931–2940

    CAS  Article  PubMed  Google Scholar 

  • Danecek P, Auton A, Abecasis G et al (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • DeSalle R, Amato G (2004) The expansion of conservation genetics. Nat Rev Genet 5:702–712

    CAS  Article  PubMed  Google Scholar 

  • Doadrio I, Dominguez O (2004) Phylogenetic relationships within the fish family Goodeidae based on cytochrome b sequence data. Mol Phylogenet Evol 31:416–430

    CAS  Article  PubMed  Google Scholar 

  • Emerson KJ, Merz CR, Catchen JM et al (2010) Resolving postglacial phylogeography using high-throughput sequencing. Proceedings of the National Academy of Sciences 107:16196–16200

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567

    Article  PubMed  Google Scholar 

  • Fischer MC, Foll M, Excoffier L, Heckel G (2011) Enhanced AFLP genome scans detect local adaptation in high-altitude populations of a small rodent (Microtus arvalis). Mol Ecol 20:1450–1462

    Article  PubMed  Google Scholar 

  • Foll M, Gaggiotti OE (2008) A genome scan method to identify selected loci appropriate for both dominant and codominant markers: A Bayesian perspective. Genetics 180:977–993

    Article  PubMed  PubMed Central  Google Scholar 

  • Foll M, Fischer MC, Heckel G, Excoffier L (2010) Estimating population structure from AFLP amplification intensity. Mol Ecol 19:4638–4647

    CAS  Article  PubMed  Google Scholar 

  • Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7:457–511

    Google Scholar 

  • Gillooly J, Brown J, West G, Savage V (2001) Effects of size and temperature on metabolic rate. Science 293.:2248–2251

  • Gilbert CH (1893) Report on the fishes of the Death Valley expedition collected in southern California and Nevada in 1891, with descriptions of new species. North Am Fauna 7:233

    Article  Google Scholar 

  • Guadalupe K (2012) Nevada Department of Wildlife native fish and amphibian field trip report XXXIII. 2:81–87

  • Hannelius U, Salmela E, Lappalainen T et al (2008) Population substructure in Finland and Sweden revealed by the use of special coordinates and a small number of unlinked autosomal SNPs. BMC Genet 9:1–12

    Article  CAS  Google Scholar 

  • Helyar SJ, Hemmer-Hansen J, Bekkevold D et al (2011) Application of SNPs for population genetics of non-model organisms:new opportunities and challenges. Mol Ecol Resour 11:123–136

    Article  PubMed  Google Scholar 

  • Hohenlohe PA, Bassham S, Etter PD et al (2010) Population genomics of parallel adaptation in threespine stickleback using sequenced RAD tags. PLoS ONE Genetics 6:1–23

    Google Scholar 

  • Houston D, Evans R, Shiozawa D (2015) Pluvial drainage patterns and Holocene desiccation influenced the genetic architecture of Relict Dace, Relictus solitarius (Teleostei: Cyprinidae). PLoS ONE 10:1–12

    CAS  Google Scholar 

  • Hubbs CL, Miller RR (1948) The zoological evidence; correlation between fish distribution and hydrographic history in the desert basins of western United States. Bull Univ Utah 38:17–166

    Google Scholar 

  • Hubbs CL, Miller RR, Hubbs LC (1974) Hydrographic history and relict fishes of the north-central Great Basin. Calif Acad Sci 7:1–259

    Google Scholar 

  • Janac M, Bryja J, Ondrackova M et al (2017) Genetic structure of three invasive gobiid species along the Danube-Rhine invasion corridor: Similar distributions, different histories. Aquat Invasions 12:551–564

    Article  Google Scholar 

  • Jelks HL, Walsh SJ, Burkhead NM et al (2008) Conservation status of imperiled North American freshwater and diadromous Fishes. Fisheries 33:372–407

    Article  Google Scholar 

  • Jombart T (2008) adegenet:a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405

    CAS  Article  PubMed  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • La Rivers I (1994) Fishes and Fisheries of Nevada. Reprint. University of Nevada Press

  • Larson WA, Seeb LW, Everett MV et al (2013) Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook Salmon (Oncorhynchus tshawytscha). Evol Appl 7:355–369

    Article  CAS  Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler Transform. Bioinformatics 25:1754–1760

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Li H, Handsaker B, Wysoker A et al (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch M (2010) Evolution of the mutation rate. Trends Genet 26:345–352

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Lyons J, Piller KR, Artigas-Azas JM et al (2019) Distribution and current conservation status of the Mexican Goodeidae (Actinopterygii, Cyprinodontiformes). ZooKeys 885:115–158

    Article  PubMed  PubMed Central  Google Scholar 

  • Martin CH, Crawford JE, Turner BJ, Simons LH (2016) Diabolical survival in Death Valley. Recent pupfish colonization, gene flow, and genetic assimilation in the smallest species range on earth. Proceedings of the Royal Society Biological Sciences 283:23–34

  • Martin CH, Höhna S (2017) New evidence for the recent divergence of Devil. ’s Hole pupfish and the plausibility of elevated mutation rates in endangered taxa. Mol Ecol 27:831–838

  • Mayr E (1942) Systematics and the Origin of Species. Columbia University Press, New York

    Google Scholar 

  • McKee EH (1971) Tertiary Igneous chronology of the Great Basin of Western United States-Implications for tectonic models. Geol Soc Am Bull 82:3497–3502

    Article  Google Scholar 

  • Meffe GK (1986) Conservation genetics and the management of endangered fishes. Fisheries 11:14–23

    Article  PubMed  PubMed Central  Google Scholar 

  • Meffe GK, Vrijenhoek RC (1988) Conservation genetics in the management of desert fishes. Conserv Biol 2:157–169

    Article  Google Scholar 

  • Miller RR, Williams JD, Williams JE (1989) Extinctions of North American fishes during the past century. Fisheries 14:22–28

    Article  Google Scholar 

  • Minckley WL, Deacon JE (1968) Southwestern fishes and the enigma of “endangered species”. Science 159:1424–1431

    CAS  Article  PubMed  Google Scholar 

  • Minckley WL, Deacon JE (1991) Battle against Extinction. Native Fish Management in the American West University of Arizona Press, Tuscon, AZ,537pp

  • Minckley WL, Marsh PC (2016) Inland fishes of the Greater Southwest: Chronicle of a vanishing biota. University of Arizona Press, Tuscon, AZ, p 478

    Google Scholar 

  • Moran P (2002) Current conservation genetics: Building an ecological approach to the synthesis of molecular and quantitative genetic methods. Ecol Freshw Fish 11:30–55

    Article  Google Scholar 

  • Morin PA, Martien KK, Taylor BL (2009) Assessing the statistical power of SNPs for population structure and conservation studies. Mol Ecol Resour 9:66–73

    CAS  Article  PubMed  Google Scholar 

  • Murphy NP, Guzik MT, Cooper SJB, Austin AD (2015) Desert spring refugia: Museums of diversity or evolutionary cradles? Zoolog Scr 44:693–701

    Article  Google Scholar 

  • Parenti LR (1981) A phylogenetic and biogeographic analysis of Cyprinodontiform fishes (Teleostei, Atherinomorpha). Bull Am Museum Nat History 168:335–357

    Google Scholar 

  • Pembleton LW, Cogan NOI, Forster JW (2013) StAMPP: an R package for calculation of genetic differentiation and structure of mixed-ploidy level populations. Mol Ecol Resour 13:946–952

    CAS  Article  PubMed  Google Scholar 

  • Planes S, Lecaillon G (1998) Consequences of the founder effect in the genetic structure of introduced island coral reef fish populations. Biol J Linn Soc 63:537–552

    Article  Google Scholar 

  • Rašić G, Filipović I, Weeks AR, Hoffmann AA (2014) Genome-wide SNPs lead to strong signals of geographic structure and relatedness patterns in the major arbovirus vector. Aedes aegypti BMC Genomics 15:1–12

    Google Scholar 

  • Reitzel AM, Herrera S, Layden MJ et al (2013) Going where traditional markers have not gone before: Utility of and promise for RAD sequencing in marine invertebrate phylogeography and population genomics. Mol Ecol 22:2953–2970

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Riddle BR, Jezkova T, Hornsby AD, Matocq MD (2014) Assembling the modern Great Basin mammal biota: Insights from molecular biogeography and the fossil record. J Mammal 95:1107–1127

    Article  Google Scholar 

  • Russello MA, Waterhouse MD, Etter PD, Johnson EA (2015) From promise to practice: Pairing non-invasive sampling with genomics in conservation. PeerJ 3. DOI https://doi.org/10.7717/peerj.1106

  • Ryman N, Utter F (1987) Population Genetics and Fisheries Management. University of Washington Press, Seattle, WA

    Google Scholar 

  • Sada DW, Vinyard GL (2002) Anthropogenic changes in biogeography of Great Basin aquatic biota. Smithson Contrib Earth Sci 33:277–293

    Google Scholar 

  • Schwartz MK, Luikart G, Waples RS (2006) Genetic monitoring as a promising tool for conservation and management. Trends in Ecology and Evolution 22:25–32

    Article  PubMed  Google Scholar 

  • Scoppettone GG, Rissler PH, Shea S (2004) A fish survey of the White River, Nevada. Western North American Naturalist 64:45–52

    Google Scholar 

  • Smith GR, Dowling TE, Gobelet KW et al (2002) Biogeography and timing of evolutionary events among Great Basin fishes. Smithson Contrib Earth Sci 33:405

    Google Scholar 

  • Smith ML (1981) Late Cenozoic fishes in the warm deserts of North America. A reinterpretation of

  • desert adaptations. Pp. 11–38 in Fishes in North American Deserts. R. J. Naiman and D. L. Soltz

  • (editors). John Wiley, New York

  • Sovic M, Fries A, Martin SA, Gibbs HL (2018) Genetic signatures of small effective population size and demographic declines in an endangered rattlesnake, Sistrurus catenatus. Evol Appl 12:664–678

    Article  CAS  Google Scholar 

  • Sumner FB, Sargent MC (1940) Some observations on the physiology of warm spring fishes. Ecology 21:45–54

    CAS  Article  Google Scholar 

  • Torres-Martinez L, Emery NC (2016) Genome-wide SNP discovery in the annual herb, Lasthenia fremontii (Asteraceae): Genetic resources for the conservation and restoration of a California vernal pool endemic. Conserv Genetic Resour 8:145–158

    Article  Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary Ne using highly variable genetic markers: A largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed  Google Scholar 

  • Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276

    CAS  Article  PubMed  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    CAS  PubMed  Google Scholar 

  • Westemeier RL, Brawn JD, Simpson SA et al (1998) Tracking the long-term decline and recovery of an isolated population. Science 282:1695–1698

    CAS  Article  PubMed  Google Scholar 

  • Wickham H (2007) Reshaping data with the reshape package. J Stat Softw 21:1–20

    Article  Google Scholar 

  • Wickham H (2016) ggplot2: Elegant graphics for data analysis. Springer-Verlag, New York, NY

    Book  Google Scholar 

  • Williams JE, Wilde GR (1981) Taxonomic status and morphology of isolated populations of the White River Springfish, Crenichthys baileyi (Cyprinodontidae). Southwest Nat 25:485–503

    Article  Google Scholar 

  • Williams CE, Williams JE (1981) Distribution and status of native fishes of the Railroad Valley system, Nevada. Transactions of the California-Nevada Section,Wildlife Society48–51

  • Willing E, Dreyer C, Oosterhout C (2012) Estimates of genetic differentiation measured by FST do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7:1–7

    Article  CAS  Google Scholar 

  • Witt J, Threloff D, Hebert P (2006) DNA barcoding reveals extraordinary cryptic diversity in an amphipod genus: Implications for desert spring conservation. Mol Ecol 15:3073–3082

    CAS  Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank the Nevada Department of Wildlife for providing the samples for this study. We would also like to thank the biologists Brandon Senger, Kevin Guadalupe, James Harter, and Mark Beckstrand for funding, support, and discussions throughout this study. Also, we would like to thank the members past and present of the Piller Lab at Southeastern Louisiana University for their continued support, advice, and assistance with this study. We would like to extend a special thanks to Jerry Kattawar III for assisting with the DNA extractions and sample preparation. The funders had no role in study design, molecular data collection and analysis, decision to publish, or preparation of the manuscript.

Funding

Funding was provided by the Nevada Department of Wildlife and the National Science Foundation (DEB 1,354,930) to KRP.

Author information

Authors and Affiliations

Authors

Contributions

DCC and KRP conceived the project idea. KRP secured the project funding. DCC performed DNA extraction and laboratory preparation of samples and was responsible for data analysis. DTC assisted with data analyses and draft editing. DCC spearheaded the writing with substantial contributions DTC and KRP.

Corresponding author

Correspondence to D. Cooper Campbell.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethics approval

Southeastern Louisiana University, IACUC 0002.

Consent for publication

All authors have consented to this papers publication.

Additional information

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.

Supplementary Material 1

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Campbell, D.C., Camak, D.T. & Piller, K.R. Islands in the desert: assessing fine scale population genomic variation of a group of imperiled desert fishes. Conserv Genet (2022). https://doi.org/10.1007/s10592-022-01457-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10592-022-01457-3

Keywords

  • Population genetics
  • Goodeidae
  • SNPs
  • Great Basin
  • Endangered species