Skip to main content
SpringerLink
Log in

Conserve the eco-evolutionary dynamic, not the subspecies: phenological divergence and gene flow between temporal cohorts of Euphilotes ancilla endemic to southern Nevada

  • Research Article
  • Published:
Conservation Genetics Aims and scope Submit manuscript

Abstract

Euphilotes ancilla purpura and cryptica (Lycaenidae), butterflies endemic to the Spring Mountains (Clark Co., Nevada), have been described as two univoltine, temporally isolated, sympatric taxa that utilize different early- and late-flowering larval host plant varieties (Eriogonum umbellatum). However, our results from field and laboratory indicate that this is not the case. The subspecies overlap in timing of adult reproductive flight (compilation of field records 1977 to 2018) and laboratory emergence of adults from early-season, non-diapause pupae indicate butterflies are not univoltine. Genetic samples collected from putative E. a. purpura (Early cohort) and cryptica (Late cohort) subpopulations show no evidence of genetic structure indicative of allochronic isolation in phylogenies of 26 mitochondrial DNA COI haplotypes and 18 nuclear ITS1 alleles. Analysis of molecular variance revealed 89% of mitochondrial DNA variation structured within and among subpopulations, with only 11% between the purportedly isolated subspecies. Analysis of isolation and migration indicated gene flow from the Early to Late cohort was 3 × greater than in the opposite direction. We conclude that, rather than two separate subspecies, Euphilotes ancilla exists in a network of partially interconnected subpopulations extending from 1750 to 3000 m across much of the Spring Mountains. Gene flow is related to the timing of adult flight and host plant flowering, contributing to the genetic variation in phenology necessary for evolutionary tracking of shifting flowering periods of larval host plants. Maintenance of connectivity and gene flow across the Spring Mountains is therefore essential for population persistence of both cohorts in the face of environmental change.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Austin GT (1998) New subspecies of Lycaenidae (Lepidoptera) from Nevada and Arizona. In: Emmel TC (ed) Systematics of western North American butterflies. Mariposa Press, Gainesville, pp 539–572

    Google Scholar 

  • Austin GT, Boyd BM, Murphy DD (2008) Euphilotes ancilla (Lycaenidae) in the Spring Mountains, Nevada: more than one species? J Lepid Soc 62:148–160

    Google Scholar 

  • Bandelt H, Forster JP, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48

    Article  CAS  PubMed  Google Scholar 

  • Braby MF, Eastwood R, Murray N (2012) The subspecies concept in butterflies: has its application in taxonomy and conservation biology outlived its usefulness? Biol J Linn Soc 106:699–716

    Article  Google Scholar 

  • Coates DJ, Byrne M, Moritz C (2018) Genetic diversity and conservation units: dealing With the species-population continuum in the age of genomics. Front Ecol Evol 6:1–13. https://doi.org/10.3389/fevo.2018.00165

    Article  Google Scholar 

  • Crandall KA, Bininda-Emonds O, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15:290–295

    Article  CAS  PubMed  Google Scholar 

  • Dixo M, Metzger JP, Morgante JS, Zamudio KR (2009) Habitat fragmentation reduces genetic diversity and connectivity among toad populations in the Brazilian Atlantic Coastal Forest. Biol Cons 142:1560–1569

    Article  Google Scholar 

  • Edelaar P, Siepielski AM, Clobert J (2008) Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution 62:2462–2472

    Article  PubMed  Google Scholar 

  • Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc B 365:3101–3112

    Article  Google Scholar 

  • Forister ML, Nice CC, Fordyce JA, Gompert Z, Shapiro AM (2008) Considering evolutionary processes in the use of single-locus genetic data for conservation, with examples from the Lepidoptera. J Insect Conserv 12:37–51

    Article  Google Scholar 

  • Forister ML, Gompert Z, Fordyce JA, Nice CC (2011) After sixty years, an answer to the question: what is the Karner blue butterfly? Biol Lett 7:399–402

    Article  PubMed  Google Scholar 

  • Funk WC, McKay JK, Hohenlohe PA, Allendorf FW (2012) Harnessing genomics for delineating conservation units. Trends Ecol Evol 27:489–496

    Article  PubMed  PubMed Central  Google Scholar 

  • Garant D, Forde SE, Hendry AP (2007) The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct Ecol 21:434–443

    Article  Google Scholar 

  • Gavrilets S (2003) Models of speciation, what have we learned in 40 years? Evolution 57:2197–2215

    Article  PubMed  Google Scholar 

  • Gradish AE, Keyghobadi N, Sperling FAH, Otis GW (2019) Population genetic structure and assessment of allochronic divergence in the Macoun’s Arctic (Oeneis macounii) butterfly Canadian. J Zool 97:121–130

    Google Scholar 

  • Haig SM, Beever EA, Chambers SM, Draheim HM, Dugger BD, Dunham S, Elliott-Smith E, Fontaine JB, Kesler DC, Knaus BJ, Lopes LF, Loschl P, Mullins TD, Sheffield LM (2006) Taxonomic considerations in listing subspecies under the U.S. Endangered Species Act. Conserv Biol 20:1584–1594

    Article  PubMed  Google Scholar 

  • Hey J, Nielsen R (2004) Multilocus methods for estimating population sizes, migration rates and divergence time, with applications to the divergence of Drosophila pseudoobscura and D. persimilis. Genetics 167:747–760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hey J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Nat Acad Sci USA 104:2785–2790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hindle BJ, Kerr CL, Richards SA, Willis SG (2015) Topographical variation reduces phenological mismatch between a butterfly and its nectar source. J Insect Conserv 19:227–236

    Article  Google Scholar 

  • Höglund J (2009) Evolutionary conservation genetics. Oxford University Press, Oxford

    Book  Google Scholar 

  • Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogeny. Bioinformatics 17:754–755

    Article  CAS  PubMed  Google Scholar 

  • Kankare M, Varkonyi G, Saccheri I (2002) Genetic differentiation between alternate-year cohorts of Xestia tecta (Lepidoptera, Noctuidae) in Finnish Lapland. Hereditas 136:169–176

    Article  PubMed  Google Scholar 

  • Kinnison MT, Hairston NG Jr (2007) Eco-evolutionary conservation biology: contemporary evolution and the dynamics of persistence. Funct Ecol 21:441–454

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh J, Bryant D (2015) POPART: full-feature software for haplotype network construction. Methods Ecol Evol 6:1110–1116

    Article  Google Scholar 

  • Mallet J (2008) Hybridization, ecological races and the nature of species: empirical evidence for the ease of speciation. Philos Trans R Soc Lond B 363:2971–2986

    Article  Google Scholar 

  • Marko PB (2011) The complex analytical landscape of gene flow inference. Trend Ecol Evol 26:448–456

    Article  Google Scholar 

  • Mee JA, Bernatchez L, Reist JD, Rogers SM, Taylor EB (2015) Identifying designatable units for intraspecific conservation prioritization: a hierarchical approach applied to the lake whitefish species complex (spp.). Evol Appl 8(5):423–441

    Article  PubMed  PubMed Central  Google Scholar 

  • Morellato LPC, Alberton B, Alvarado ST, Borges B, Buisson E, Camargo MGG, Cancian LF, Carstensen DW, Escobar DFE, Leite PTP, Mendoza I, Rocha NMWB, Soares NC, Silva TSF, Staggemeier VG, Streher AS, Vargas BC, Peres CA (2016) Linking plant phenology to conservation biology. Biol Conserv 195:60–72

    Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    Article  PubMed  Google Scholar 

  • Nicolaus M, Edelaar P (2018) Comparing the consequences of natural selection, adaptive phenotypic plasticity, and matching habitat choice for phenotype–environment matching, population genetic structure, and reproductive isolation in meta-populations. Ecol Evol 8:3815–3827

    Article  PubMed  PubMed Central  Google Scholar 

  • Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896

    CAS  PubMed  PubMed Central  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Ann Rev Ecol Syst 37:637–669

    Article  Google Scholar 

  • Patten MA (2015) Subspecies and the philosophy of science. The Auk 132(2):481–485

    Article  Google Scholar 

  • Patten MA, Unitt P, Sheldon F (2002) Diagnosability versus mean differences of sage sparrow subspecies. The Auk 119(1):26–35

    Article  Google Scholar 

  • Pavlova A, Selwood P, Harrisson KA, Murray N, Quin B, Menkhorst P, Smales I, Sunnucks P (2014) Integrating phylogeography and morphometrics to assess conservation merits and inform conservation strategies for an endangered subspecies of a common bird species. Biol Conserv 174:136–146

    Article  Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlEx 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Peakall R, Smouse PE (2012) GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research – an update. Bioinformatics 28:2537–2539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peterson M (1995) Phenological isolation, gene flow, and developmental differences among low- and high-elevation populations of Euphilotes enoptes (Lepidoptera: Lycaeidae). Evolution 49:446–455

    Article  PubMed  Google Scholar 

  • Peterson M (1997) Host plant phenology and butterfly dispersal: causes and consequences of uphill movement. Ecology 78:167–180

    Article  Google Scholar 

  • Phillimore A, Owens I (2006) Are subspecies useful in evolutionary and conservation biology? . Proc R Soc B 273:1049–1053

    Article  PubMed  PubMed Central  Google Scholar 

  • Pollard E, Yates T (1993) Monitoring butterflies for ecology and conservation. Chapman and Hall, Boca Raton

    Google Scholar 

  • Pratt GF (1988) The evolution and biology of Euphilotes biotypes [thesis]. University of California Riverside, Riverside, CA

  • Pratt GF (1994) Evolution of Euphilotes (Lepidoptera: Lycaenidae) by seasonal and host shifts. Biol J Linn Soc 51:387–416

    Article  Google Scholar 

  • Pratt GF, Ballmer GR (1986) The phenetics and comparative biology of Euphilotes enoptes (Boisduval) (Lycaenidae) from the San Bernardino Mountains. J Lepid Soc 25:121–135

    Google Scholar 

  • Prentice MB, Bowman J, Murray DL, Klütsch C, Wilson PJ (2019) Evaluating evolutionary history and adaptive differentiation to identify conservation units of Canada lynx (Lynx canadensis). Glob Ecol Cons 20:1–16

    Google Scholar 

  • Pressey RL, Cabeza M, Watts ME, Cowling RM, Wilson KA (2007) Conservation planning in a changing world. Trends Ecol Evol 22:583–592

    Article  PubMed  Google Scholar 

  • Ravigné V, Dieckmann U, Olivieri I (2009) Live where you thrive: joint evolution of habitat choice and local adaptation facilitates specialization and promotes diversity. Am Nat 174:141–169

    Article  Google Scholar 

  • Ratnasingham S, Hebert PDN (2007) BOLD: The Barcode of Life Data System (www.barcodinglife.org). Mol Ecol Notes 7:355–364

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sackett LC, Seglund A, Guralnick RP, Mazzella MM, Wagner DM, Busch JD, Martin AP (2014) Evidence for two subspecies of Gunnison’s prairie dogs (Cynomys gunnisoni) and the general importance of the subspecies concept. Biol Conserv 174:1–11

    Article  Google Scholar 

  • Santos H, Burban C, Rousselet J, Rossi JP, Branco M, Kerdelhu C (2011) Incipient allochronic speciation in the pine processionary moth (Thaumetopoea pityocampa, Lepidoptera, Notodontidae). J Evol Biol 24:146–158

    Article  CAS  PubMed  Google Scholar 

  • Schliep KP (2011) phangorn: phylogenetic analysis in R. Bioinformatics 27:592–593

    Article  CAS  PubMed  Google Scholar 

  • Servedio MR, Noor MAF (2003) The role of reinforcement in speciation: theory and data. Ann Rev Ecol Evol Syst 34:339–364

    Article  Google Scholar 

  • Servedio MR, Doorn GSV, Kopp M, Frame AM, Nosil P (2011) Magic traits in speciation: magic but not rare? Trends Ecol Evol 26:389–397

    Article  PubMed  Google Scholar 

  • Shaffer HB (2013) Evolution and conservation. In: Losos J (ed) The Princeton guide to evolution. Princeton University Press, Princeton, pp 766–773

    Chapter  Google Scholar 

  • Sherry RA, Zhou X, Gu S, Arnone JA, Schimel DS, Verburg PS, Wallace LL, Luo Y (2007) Divergence of reproductive phenology under climate warming. Proc Nat Acad Sci USA 104:198–202

    Article  CAS  PubMed  Google Scholar 

  • Smadja CM, Butlin RK (2011) A framework for comparing processes of speciation in the presence of gene flow. Mol Ecol 20:5123–5140

    Article  PubMed  Google Scholar 

  • Stockwell CA, Hendry AP, Kinnison MT (2003) Contemporary evolution meets conservation biology. Trend Ecol Evol 18:94–101

    Article  Google Scholar 

  • Taylor EB, Darveau C, Schulte PM (2013) Setting conservation priorities in a widespread species: phylogeographic and physiological variation in the Lake Chub, Couesius plumbeus (Pisces: Cyprinidae). Diversity 5:149–165

    Article  Google Scholar 

  • Ugelvig LV, Vila R, Pierce NE, Nash DR (2011) A phylogenetic revision of the Glaucopsyche section (Lepidoptera: Lycaenidae), with special focus on the Phengaris–Maculinea clade. Mol Phylogenet Evol 61:237–243

    Article  CAS  PubMed  Google Scholar 

  • USFWS (2012) Endangered and threatened wildlife and plants; 90-day finding on petitions to list the two Spring Mountains dark blue butterflies and Morand’s checkerspot butterfly as endangered or threatened. Department of the Interior, Fish and Wildlife Service August 7, 2012 Federal Register 77:47003–47011

  • Wadgymar SM, Weis AE (2017) Phenological mismatch and the effectiveness of assisted gene flow. Conserv Biol 31(3):547–558

    Article  PubMed  Google Scholar 

  • Wilson JS, Sneck M, Murphy DD, Nice CC, Fordyce JA, Forister ML (2013) Complex evolutionary history of the pallid dotted-blue butterfly (Lycaenidae: Euphilotes pallescens) in the Great Basin of western North America. J Biogeogr 40:2059–2070

    Article  Google Scholar 

  • Yamamoto S, Sota T (2009) Incipient allochronic speciation by climatic disruption of the reproductive period. Proc R Soc Lond B 276:2711–2271

    Article  Google Scholar 

  • Zhang J, Cong Q, Shen J, Opler PA, Grishin NV (2019) Genomics of a complete butterfly continent. BioRxiv.https://doi.org/10.1101/829887

    Article  Google Scholar 

  • Zink RM (2004) The role of subspecies in obscuring avian biological diversity and misleading conservation policy. Proc R Soc Lond B 271:561–564

    Article  Google Scholar 

Download references

Acknowledgements

This project would not have been possible without the assistance and input of a large number of individuals including (alphabetical order): C. Anderson, G. Benito, J. Brickey, N. Carvajal Acosta, J. Hansen, J. Hurja, E. Jones, M. Mountain, A. Nichols, K. O’Connor, A. Reed, E. Rhodes, M. Salcido, H. Steven, G. Varella, S. Walker, W. Welch, and D. Yost. We also thank M. Forister and J. Wilson who graciously provided DNA samples from a published dataset of Euphilotes in Nevada and also provided advice on sequencing. The manuscript was improved by the comments of G. Pratt and two anonymous reviewers. Funding for this research was provided by the U.S. Fish and Wildlife Service (Southern Nevada) and U.S. Forest Service (Humboldt-Toiyabe National Forest). The findings and conclusions in this article are those of the author(s) and do not necessarily represent the views of the U.S. Fish and Wildlife Service or U.S. Forest Service.

Funding

Funding was provided by U.S. Fish and Wildlife Service (Grant No. F14AC00613) and U.S. Forest Service (Grant No. AG-9360-S-10-0001).

Author information

Authors and Affiliations

  1. School of Life Sciences, University of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, NV, 89154, USA

    Daniel B. Thompson

  2. Rocky Mountain Research Station, Wildlife and Terrestrial Ecosystems Forest Service, 800 East Beckwith, Missoula, MT, 59801, USA

    Kevin McKelvey & Kristine L. Pilgrim

  3. Groningen Institute for Evolutionary Life Sciences, University of Groningen, PO Box 11103, 9700 CC, Groningen, The Netherlands

    Paul van Els

  4. Geosciences, University of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, NV, 89154, USA

    Gretchen Andrew

  5. Adelson Educational Campus, 9700 Hillpointe Road, Las Vegas, NV, 89134, USA

    Paula Jacoby-Garrett

  6. Nevada Department of Wildlife, 60 Youth Center Road, Elko, NV, 89801, USA

    Matt Glenn

  7. U.S. Fish and Wildlife Service, 4701 N. Torrey Pines Dr., Las Vegas, NV, 89130, USA

    Corey Kallstrom

  8. Department of Bioagricultural Sciences, C.P. Gillette Museum of Arthropod Diversity, Colorado State University, Fort Collins, CO, 80523-1177, USA

    Paul A. Opler

Authors
  1. Daniel B. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kevin McKelvey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Paul van Els
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Gretchen Andrew
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Paula Jacoby-Garrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Matt Glenn
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Corey Kallstrom
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Kristine L. Pilgrim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Paul A. Opler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Daniel B. Thompson.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Thompson, D.B., McKelvey, K., van Els, P. et al. Conserve the eco-evolutionary dynamic, not the subspecies: phenological divergence and gene flow between temporal cohorts of Euphilotes ancilla endemic to southern Nevada. Conserv Genet 21, 341–357 (2020). https://doi.org/10.1007/s10592-020-01254-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-020-01254-w

Keywords

Search

Navigation