Climate-driven range shift prompts species replacement

Abstract

Climate change prompts warm-tolerant species upward and poleward to either displace or replace cold-tolerant species. Warm-tolerant species may replace cold-tolerant individuals with upward migration, or cold-tolerant genes if the species hybridize. We examined genetic and morphological differences between low elevation, warm-tolerant (Aphaenogaster rudis) and high elevation cold-tolerant (A. picea) ant species that form an upward-shifting ecotone in the southern Appalachian Mountains (USA). The A. picea/A. rudis ecotone shifted upward ca. 200 m between the decades 1970 and 2010, and characteristic morphological traits appeared muddled where the species met, suggesting hybridization. However, we found no evidence of genetic hybridization, and the trait most associated with species identity, pigmentation, remained so across the environmental gradients. Conversely, femur length did not differentiate well between species identities, and it shifted across the environmental gradients. These results suggest that the cold tolerant A. picea, associated with high-elevation and high-latitude, was replaced by the warm-tolerant, low elevation A. rudis species. As such, these results suggest that less competitive cold-tolerant species may be replaced by more competitive cold-intolerant species with climate warming.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Brady SG, Schultz TR, Fisher BL, Ward PS (2006) Evaluating alternative hypotheses for the early evolution and diversification of ants. Proc Natl Acad Sci USA 273:1643–1649

    Google Scholar 

  2. Brommer JE (2004) The range margins of northern birds shifts polewards. Ann Zool 41:391–397

    Google Scholar 

  3. Bruce RC (2007) Out of the frying pan into the fire: an ecological perspective on evolutionary reversal in life history in plethodontid salamanders (Amphibia: Plethodontidae). Evol Ecol 21:703–726

    Article  Google Scholar 

  4. Buggs RJA (2007) Empirical study of hybrid zone movement. Heredity 99:301–312

    CAS  Article  PubMed  Google Scholar 

  5. Cahan SH, Keller L (2003) Complex hybrid origin of genetic caste determination in harvester ants. Nature 424:306–309

    Article  Google Scholar 

  6. Castoe TA, Doan TM, Parkinson CL (2004) Data partitions and complex models in Bayesian analysis: the phylogeny of gymnophthalmid lizards. Syst Biol 53:448–469

    Article  PubMed  Google Scholar 

  7. Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago, Chicago

    Book  Google Scholar 

  8. Connell JH (1975) Some mechanisms producing structure in natural communities: a model and evidence from field experiments. In: Cody ML, Diamond JM (eds) Ecology and evolution of communities. Harvard University Press, Cambridge, pp 460–490

    Google Scholar 

  9. Creighton WS (1950) The ants of North America, vol 104. Bull Mus Comp Zool. The Cosmos Press, Inc., Cambridge

  10. Crozier RH (1977) Genetic differentiation between populations of the ant Aphaenogaster ‘rudis’ in the southeastern United States. Genetica 47:17–36

    Article  Google Scholar 

  11. De Marco B, Cognato AI (2016) A multiple gene phylogeny reveals polyphyly among eastern North American Aphaenogaster species (Hymenoptera: Formicidae). Zool Scrip. doi:10.1111/zsc.12168

    Google Scholar 

  12. Delcourt HR, Delcourt PA (1987) Long-term forest dynamics of the temperate zone. Springer, New York

    Book  Google Scholar 

  13. Delcourt HR, Delcourt PA (2000) Eastern deciduous forests. In: Barbour MG, Billings WD (eds) North American terrestrial vegetation. Cambridge University Press, Cambridge

    Google Scholar 

  14. Dunn RR, Parker CR, Sanders NJ (2007) Temporal patterns of diversity: assessing the biotic and abiotic controls on ant assemblages. Biol J Linn Soc 91:191–201

    Article  Google Scholar 

  15. Ellers J, Boggs CL (2004) Functional ecological implications of intraspecific differences in wing melanization in Colias butterflies. Biol J Linn Soc 82:79–87

    Article  Google Scholar 

  16. Ellison AM, Gotelli NJ, Farnsworth EJ, Alpert GD (2012) A field guide to the ants of New England. Yale University Press, New Haven

    Google Scholar 

  17. Greiner B, Narendra A, Reid SF, Dacke M, Ribi WA, Zeil J (2007) Eye structure correlates with distinct foraging-bout timing in primitive ants. Curr Biol 17:R879–R880

    CAS  Article  PubMed  Google Scholar 

  18. Hairston NG (1949) The local distribution and ecology of the Plethodontid salamanders of the Southern Appalachians. Ecol Monogr 19:49–73

    Article  Google Scholar 

  19. Hairston NG (1951) Interspecies competition and its probable influence upon the vertical distribution of Appalachian salamanders of the genus Plethodon. Ecology 32:266–274

    Article  Google Scholar 

  20. Hairston NG, Wiley RH, Smith CK, Kneidel KA (1992) The dynamics of two hybrid zones in Appalachian salamanders of the genus Plethodon. Evolution 46:930–938

    Article  Google Scholar 

  21. Harr B, Price T (2014) Climate change: a hybrid zone moves north. Curr Biol 24:230–232

    Article  Google Scholar 

  22. Highton R, Peabody RB (2000) Geographic protein variation and speciation in salamanders of the Plethodon jordani and Plethodon glutinosus complexes in the southern Appalachian mountains with the description of four new species. In: Bruce RC, Jaeger RG, Houck LD (eds) The biology of Plethodontid Salamanders. Kluwer Academic/Plenum, New York

    Google Scholar 

  23. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17:754–755

    CAS  Article  PubMed  Google Scholar 

  24. Hurlbert SH, Lombardi CM (2009) Final collapse of the Newman-Pearson decision theoretic framework and the rise of the neoFisherian. Ann Zool 46:311–349

    Article  Google Scholar 

  25. Ibanez I, Clark JS, Dietze MC (2008) Evaluating the sources of potential migrant species: implications under climate change. Ecol Appl 18:1664–1678

    Article  PubMed  Google Scholar 

  26. Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99:8157–8160

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  27. Kaspari M, Clay NA, Lucas J, Yanoviak SP, Kay A (2015) Thermal adaptation generates a diversity of thermal limits in a rainforest ant community. Glob Change Biol 21:1092–1102

    Article  Google Scholar 

  28. Kelly AE, Goulden ML (2008) Rapid shifts in plant distribution with recent climate change. Proc Natl Acad Sci USA 105:11823–11826

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  29. King JR, Warren RJ II, Bradford MA (2013) Social insects dominate eastern US temperate hardwood forest macroinvertebrate communities in warmer regions. PLoS One 8:e75843

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  30. Lubertazzi D (2012) The biology and natural history of Aphaenogaster rudis. Psyche 2012:752815

    Article  Google Scholar 

  31. Menge BA, Sutherland JP (1987) Community regulation—variation in disturbance, competition, and predation in relation to environmental-stress and recruitment. Am Nat 130:730–757

    Article  Google Scholar 

  32. Miller MA, Pfeiffer W, Schwartz T (2010) Creating the CIPRES science gateway for inference of large phylogetic trees. In: Proceedings of the gateway computing environment workshop (GCE), New Orleans, LA, USA

  33. Miller-Rushing AJ, Lloyd-Evans TL, Primack RB, Satzinger P (2008) Bird migration times, climate change, and changing population sizes. Glob Change Biol 14:1959–1972

    Article  Google Scholar 

  34. MontBlanc EM, Chambers JC, Brussard PF (2007) Variation in ant populations with elevation, tree cover, and fire in a pinyon-juniper-dominated watershed. West N Am Nat 67:469–491

    Article  Google Scholar 

  35. Ness JH, Morin DF, Giladi I (2009) Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists? Oikos 12:1793–1804

    Article  Google Scholar 

  36. Nylander JAA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey J (2004) Bayesian phylogenetic analysis of combined data. Syst Biol 53:47–67

    Article  PubMed  Google Scholar 

  37. Parkash R, Munjal AK (1999) Phenotypic variability of thoracic pigmentation in Indian populations of Drosophila melanogaster. J Zool Syst Evol Res 37:133–140

    Article  Google Scholar 

  38. Parmesan C et al (1999) Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 399:579–583

    CAS  Article  Google Scholar 

  39. Parr CL, Gibb H (2009) Competition and the role of dominant ants. In: Lach L, Parr CL, Abbott KL (eds) Ant ecology. Oxford University Press, Oxford, pp 77–96

    Google Scholar 

  40. Pearce-Duvet JMC, Elemans CPH, Feener DH Jr (2011) Walking the line: search behavior and foraging success. Behav Ecol 22:501–509

    Article  Google Scholar 

  41. Pelini SL, Dzurisin JDK, Prior KM, Williams CM, Marsico TD, Sinclair BJ, Hellmann JJ (2009) Translocation experiments with butterflies reveal limits to enhancement of poleward populations under climate change. Proc Natl Acad Sci USA 106:11160–11165

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  42. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distributional shifts in marine fishes. Science 308:1912–1915

    CAS  Article  PubMed  Google Scholar 

  43. R Development Core Team (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  44. Robinson CH (2001) Cold adaptation in Arctic and Antarctic fungi. New Phytol 151:341–353

    CAS  Article  Google Scholar 

  45. Sanders NJ, Lessard JP, Fitzpatrick MC, Dunn RR (2007) Temperature, but not productivity or geometry, predicts elevational diversity gradients in ants across spatial grains. Glob Ecol Biogeogr 16:640–649

    Article  Google Scholar 

  46. Schweiger O, Settele J, Kudrna O, Klotz S, Kuhn I (2008) Climate change can cause spatial mismatch of trophically interacting species. Ecology 89:3472–3479

    Article  PubMed  Google Scholar 

  47. Seifert B (2009) Cryptic species in ants (Hymentoptera: Formicidae) revisited: we need a change in the alpha-taxonomic approach. Myrmecol News 12:149–166

    Google Scholar 

  48. Shoemaker DD, Ross KG, Arnold ML (1996) Genetic structure and evolution of a fire ant hybrid zone. Evolution 50:1958–1976

    Article  Google Scholar 

  49. Tilman D, Pascala S (1993) The maintenance of species richness in plant communities. In: Ricklefs RE, Schluter R (eds) Species diversity in ecological communities. University of Chicago Press, Chicago

    Google Scholar 

  50. Umphrey GJ (1996) Morphometric discrimination among sibling species in the fulva-rudis-texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae). Can J Zool 74:528–559

    Article  Google Scholar 

  51. Urban MC, Tewksbury JJ, Sheldon KS (2012) On a collision course: competition and dispersal differences create no-analogue communities and cause extinctions during climate change. Proc R Soc B Biol Sci 279:2072–2080

    Article  Google Scholar 

  52. Ward PS, Brady SG, Fisher BL, Schultz TR (2010) Phylogeny and biogeography of dolichoderine ants: effects of data partitioning and relict taxa on historical inference. Syst Biol 59:342–362

    CAS  Article  PubMed  Google Scholar 

  53. Warren RJ II, Bradford MA (2013) Mutualism fails when climate response differs between interacting species. Glob Change Biol 20:466–474

    Article  Google Scholar 

  54. Warren RJ II, Chick L (2013) Upward ant distribution shift corresponds with minimum, not maximum, temperature tolerance. Glob Change Biol 19:2082–2088

    Article  Google Scholar 

  55. Warren RJ II, Bahn V, Bradford MA (2011a) Temperature cues phenological synchrony in ant-mediated seed dispersal. Glob Change Biol 17:2444–2454

    Article  Google Scholar 

  56. Warren RJ II, McAfee P, Bahn V (2011b) Ecological differentiation among key plant mutualists from a cryptic ant guild. Insect Soc 58:505–512

    Article  Google Scholar 

  57. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053

    Article  Google Scholar 

  58. Zhu K, Woodall CW, Ghosh S, Gelfand AE, Clark JS (2013) Dual impacts of climate change: forest migration and turnover through life history. Glob Change Biol 20:251–264

    Article  Google Scholar 

  59. Zuckerberg B, Woods AM, Porter W (2009) Poleward shifts in breeding bird distributions in New York State. Glob Change Biol 15:1866–1883

    Article  Google Scholar 

Download references

Acknowledgments

Partial support for this research was provided by the SUNY Buffalo State Office of Undergraduate Research. Additional funding was provided to LDC through National Science Foundation Grant 1136703—Dimensions in Biodiversity: Collaborative Research: The climate cascade: functional and evolutionary consequences of climatic change on species, trait, and genetic diversity in a temperate ant community to PIs: Nate Sanders, Aaron Ellison, Nick Gotelli, Sara Helms Cahan, Bryan Ballif, and Rob Dunn. We also thank Highlands Biological Stations Director Jim Costa and staff for support; Victor Agraz, Deborah Jackson, Mary Schultz, Chris Broecker, Havish Deepnarain, Nicole Dexter, Jesse Helton, Jing Niu, Vidhyaben Patel, Zeph Pendleton, Rachel Power, Paula Reith, Morgan Spinelli for field help. We thank the Georgia Department of Natural Resources Nongame Conservation Section and the US Forest Service Chattahoochee-Oconee National Forest for permission to collect ants. We also thank Georgia Museum of Natural History Curator and Collections Manager Richard Hoebeke for loaning us Aphaenogaster specimens from R. H. Crozier’s collections.

Author information

Affiliations

Authors

Corresponding author

Correspondence to R. J. Warren II.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 168 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Warren, R.J., Chick, L.D., DeMarco, B. et al. Climate-driven range shift prompts species replacement. Insect. Soc. 63, 593–601 (2016). https://doi.org/10.1007/s00040-016-0504-0

Download citation

Keywords

  • Aphaenogaster
  • Rudis complex
  • Hybridization
  • Traits
  • Phenotypic plasticity
  • Phylogenetics