Invasive exotic species are spreading rapidly throughout the planet. These species can have widespread impacts on biodiversity, yet the ability for native species, particularly long-lived vertebrates, to respond rapidly to invasions remains mostly unknown. Here we provide evidence of rapid morphological change in the endangered snail kite (Rostrhamus sociabilis) across its North American range with the invasion of a novel prey, the island apple snail (Pomacea maculata), a much larger congener of the kite’s native prey. In less than one decade since invasion, snail kite bill size and body mass increased substantially. Larger bills should be better suited to extracting meat from the larger snail shells, and we detected strong selection on increased size through juvenile survival. Using pedigree data, we found evidence of both genetic and environmental influences on trait expression and discovered that additive genetic variation in bill size increased with invasion. However, trends in predicted breeding values emphasize that recent morphological changes have been driven primarily by phenotypic plasticity rather than micro-evolutionary change. Our findings suggest that evolutionary change may be imminent and underscore that even long-lived vertebrates can respond quickly to invasive species. Furthermore, these results highlight that phenotypic plasticity may provide a crucial role for predators experiencing rapid environmental change.
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Vitousek, P. M., D'Antonio, C. M., Loope, L. L., Rejmanek, M. & Westbrooks, R. Introduced species: a significant component of human-caused global change. N. Z. J. Ecol. 21, 1–16 (1997).
Maron, J. L., Vila, M., Bommarco, R., Elmendorf, S. & Beardsley, P. Rapid evolution of an invasive plant. Ecol. Monogr. 74, 261–280 (2004).
Hanfling, B. & Kollmann, J. An evolutionary perspective of biological invasions. Trends Ecol. Evol. 17, 545–546 (2002).
Shine, R. Invasive species as drivers of evolutionary change: cane toads in tropical Australia. Evol. Appl. 5, 107–116 (2012).
Sih, A., Ferrari, M. C. O. & Harris, D. J. Evolution and behavioural responses to human-induced rapid environmental change. Evol. Appl. 4, 367–387 (2011).
Moran, E. V. & Alexander, J. M. Evolutionary responses to global change: lessons from invasive species. Ecol. Lett. 17, 637–649 (2014).
Henle, K., Davies, K. F., Kleyer, M., Margules, C. & Settele, J. Predictors of species sensitivity to fragmentation. Biodivers. Conserv. 13, 207–251 (2004).
Carroll, S. P. et al. And the beak shall inherit — evolution in response to invasion. Ecol. Lett. 8, 944–951 (2005).
Prentis, P. J., Wilson, J. R. U., Dormontt, E. E., Richardson, D. M. & Lowe, A. J. Adaptive evolution in invasive species. Trends Plant Sci. 13, 288–294 (2008).
Langkilde, T. Invasive fire ants alter behavior and morphology of native lizards. Ecology 90, 208–217 (2009).
Estes, J. A. et al. Trophic downgrading of planet Earth. Science 333, 301–306 (2011).
Berthon, K. How do native species respond to invaders? Mechanistic and trait-based perspectives. Biol. Invasions 17, 2199–2211 (2015).
Phillips, B. L. & Shine, R. Adapting to an invasive species: toxic cane toads induce morphological change in Australian snakes. Proc. Natl Acad. Sci. USA 101, 17150–17155 (2004).
Hayes, K. A., Cowie, R. H., Thiengo, S. C. & Strong, E. E. Comparing apples with apples: clarifying the identities of two highly invasive neotropical Ampullariidae (Caenogastropoda). Zool. J. Linn. Soc. 166, 723–753 (2012).
Reichert, B. E. et al. in The Birds of North America Online (ed. Poole, A.) https://doi.org/10.2173/bna.171 (Cornell Lab of Ornithology, Ithaca, 2015).
Rawlings, T. A., Hayes, K. A., Cowie, R. H. & Collins, T. M. The identity, distribution, and impacts of non-native apple snails in the continental United States. BMC Evol. Biol. 7, 97 (2007).
Cattau, C. E., Fletcher, R. J. Jr, Reichert, B. E. & Kitchens, W. M. Counteracting effects of a non-native prey on the demography of a native predator culminate in positive population growth. Ecol. Appl. 26, 1952–1968 (2016).
Darby, P. C., Mellow, D. J. & Watford, M. L. Food-handling difficulties for snail kites capturing non-native apple snails. Fla. Field Nat. 35, 79–85 (2007).
Cattau, C. E., Martin, J. & Kitchens, W. M. Effects of an exotic prey species on a native specialist: example of the snail kite. Biol. Conserv. 143, 513–520 (2010).
Martin, J., Kitchens, W. M., Cattau, C. E. & Oli, M. K. Relative importance of natural disturbances and habitat degradation on snail kite population dynamics. Endanger. Species Res. 6, 25–39 (2008).
Saul, W.-C. & Jeschke, J. M. Eco-evolutionary experience in novel species interactions. Ecol. Lett. 18, 236–245 (2015).
Wilcox, R. & Fletcher, R. J. Jr. Experimental test of preferences for an invasive prey by an endangered predator: implications for conservation. PLoS ONE 11, e0165427 (2016).
Snyder, N. F. R. & Snyder, H. A. A comparative study of mollusk predastion by limpkins, Everglade kites, and boat-tailed grackles. Living Bird 8, 177–223 (1969).
Sykes, P. W. Jr. The feeding habits of the snail kite in Florida, USA. Colon. Waterbirds 10, 84–92 (1987).
Strauss, S. Y., Lau, J. A. & Carroll, S. P. Evolutionary responses of natives to introduced species: what do introductions tell us about natural communities? Ecol. Lett. 9, 354–371 (2006).
Stockwell, C. A., Hendry, A. P. & Kinnison, M. T. Contemporary evolution meets conservation biology. Trends Ecol. Evol. 18, 94–101 (2003).
Lande, R. & Arnold, S. J. The measurement of selection on correlated characters. Evolution 37, 1210–1226 (1983).
Morrissey, M. B. & Sakrejda, K. Unification of regression-based methods for the analysis of natural selection. Evolution 67, 2094–2100 (2013).
Kruuk, L. E. B. Estimating genetic parameters in natural populations using the ‘animal model’. Phil. Trans. R. Soc. Lond. B 359, 873–890 (2004).
Wilson, A. J. et al. An ecologist’s guide to the animal model. J. Anim. Ecol. 79, 13–26 (2010).
Merila, J. & Hendry, A. P. Climate change, adaptation, and phenotypic plasticity: the problem and the evidence. Evol. Appl. 7, 1–14 (2014).
Hansen, T. F., Pelabon, C. & Houle, D. Heritability is not evolvability. Evol. Biol. 38, 258–277 (2011).
Gibson, G. & Dworkin, I. Uncovering cryptic genetic variation. Nat. Rev. Genet. 5, 681–690 (2004).
Hadfield, J. D., Wilson, A. J., Garant, D., Sheldon, B. C. & Kruuk, L. E. B. The misuse of BLUP in ecology and evolution. Am. Nat. 175, 116–125 (2010).
Falconer, S. & Mackay, T. F. C. Introduction to Quantitative Genetics 4th edn (Pearson Education, Harlow, 1996).
Mooney, H. A. & Cleland, E. E. The evolutionary impact of invasive species. Proc. Natl Acad. Sci. USA 98, 5446–5451 (2001).
Lande, R. & Shannon, S. The role of genetic variation in adaptation and population persistence in a changing environment. Evolution 50, 434–437 (1996).
Paaby, A. B. & Rockman, M. V. Cryptic genetic variation: evolution’s hidden substrate. Nat. Rev. Genet. 15, 247–258 (2014).
West-Eberhard, M. J. Developmental Plasticity and Evolution (Oxford Univ. Press, New York, 2003).
Postma, E. Implications of the difference between true and predicted breeding values for the study of natural selection and micro-evolution. J. Evol. Biol. 19, 309–320 (2006).
Merila, J., Kruuk, L. E. B. & Sheldon, B. C. Natural selection on the genetical component of variance in body condition in a wild bird population. J. Evol. Biol. 14, 918–929 (2001).
Reale, D., McAdam, A. G., Boutin, S. & Berteaux, D. Genetic and plastic responses of a northern mammal to climate change. Proc. R. Soc. Lond. B 270, 591–596 (2003).
Morrissey, M. B., Kruuk, L. E. B. & Wilson, A. J. The danger of applying the breeder’s equation in observational studies of natural populations. J. Evol. Biol. 23, 2277–2288 (2010).
Beissinger, S. R. & Snyder, N. F. R. Mate desertion in the snail kite. Anim. Behav. 35, 477–487 (1988).
Lacombe, D., Bird, D. M. & Hibbard, K. A. Influence of reduced food availability on growth of captive American kestrels. Can. J. Zool. 72, 2084–2089 (1994).
Reichert, B. E., Kendall, W. L., Fletcher, R. J. Jr. & Kitchens, W. M. Spatio-temporal variation in age structure and abundance of the endangered snail kite: pooling across regions masks a declining and aging population. PLoS ONE 11, e0162690 (2016).
Griffith, S. C., Owens, I. P. F. & Thuman, K. A. Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol. Ecol. 11, 2195–2212 (2002).
Mougeot, F. Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis. Anim. Behav. 67, 1067–1076 (2004).
Charmantier, A. & Reale, D. How do misassigned paternities affect the estimation of heritability in the wild? Mol. Ecol. 14, 2839–2850 (2005).
Firth, J. A., Hadfield, J. D., Santure, A. W., Slate, J. & Sheldon, B. C. The influence of nonrandom extra-pair paternity on heritability estimates derived from wild pedigrees. Evolution 69, 1336–1344 (2015).
Darby, P. C., Fujisaki, I. & Mellow, D. J. The effects of prey density on capture times and foraging success of course-hunting adult snail kites. Condor 114, 755–763 (2012).
Hespenheide, H. A. Ecological inferences from morphological data. Annu. Rev. Ecol. Syst. 4, 213–229 (1973).
Grant, P. R. & Grant, B. R. Unpredictable evolution in a 30-year study of Darwin’s finches. Science 296, 707–711 (2002).
Tornberg, R., Monkkonen, M. & Pahkala, M. Changes in diet and morphology of Finnish goshawks from 1960s to 1990s. Oecologia 121, 369–376 (1999).
Robertson, E. P., Fletcher, R. J. Jr & Austin, J. D. Microsatellite polymorphism in the endangered snail kite reveals a panmictic, low diversity population. Conserv. Genet. https://doi.org/10.1007/s10592-017-1003-1 (2017).
Bennetts, R. E. & Kitchens, W. M. Factors influencing movement probabilities of a nomadic food specialist: proximate foraging benefits or ultimate gains from exploration? Oikos 91, 459–467 (2000).
Reichert, B. E., Fletcher, R. J. Jr, Cattau, C. E. & Kitchens, W. M. Consistent scaling of population structure across landscapes despite intraspecific variation in movement and connectivity. J. Anim. Ecol. 85, 1563–1573 (2016).
Snyder, N. F. R., Beissinger, S. R. & Chandler, R. E. Reproduction and demography of the Florida Everglade (snail) kite. Condor 91, 300–316 (1989).
Rising, J. D. & Somers, K. M. The measurement of overall body size in birds. Auk 106, 666–674 (1989).
Newton, I. Population Ecology of Raptors (Poyser, London, 1979).
Field, D. J., Lynner, C., Brown, C. & Darroch, S. A. F. Skeletal correlates for body mass estimation in modern and fossil flying birds. PLoS ONE 8, e82000 (2013).
Price, T., Kirkpatrick, M. & Arnold, S. J. Directional selection and the evolution of breeding date in birds. Science 240, 798–799 (1988).
Beissinger, S. R. Mate Desertion and Reproductive Effort in the Snail Kite. PhD thesis, Univ. Michigan (1984).
Vannoordwijk, A. J., Vanbalen, J. H. & Scharloo, W. Heritability of body size in a natural population of the great tit (Parus major) and its relation to age and environmental conditions during growth. Genet. Res. 51, 149–162 (1988).
R Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, 2016).
Martin, J., Kitchens, W. M. & Hines, J. E. Natal location influences movement and survival of a spatially structured population of snail kites. Oecologia 153, 291–301 (2007).
Kingsolver, J. G. et al. The strength of phenotypic selection in natural populations. Am. Nat. 157, 245–261 (2001).
Wood, S. N. Generalized Additive Models: an Introduction with R (Chapman & Hall and CRC, Boca Raton, 2006).
Charmantier, A. & Garant, D. Environmental quality and evolutionary potential: lessons from wild populations. Proc. R. Soc. B 272, 1415–1425 (2005).
Stubben, C. & Milligan, B. Estimating and analyzing demographic models using the popbio package in R. J. Stat. Softw. 22, 1–23 (2007).
We thank J. Orrock, B. Reichert, E. Robertson and M. Morrissey for providing comments on earlier versions of this manuscript. This project was funded by USGS’s Greater Everglades Priority Ecosystems Science (GEPES), the US Army Corps of Engineers, and US Fish and Wildlife Service.
The authors declare no competing financial interests.
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
About this article
Cite this article
Cattau, C.E., Fletcher Jr, R.J., Kimball, R.T. et al. Rapid morphological change of a top predator with the invasion of a novel prey. Nat Ecol Evol 2, 108–115 (2018). https://doi.org/10.1038/s41559-017-0378-1
Rapid responses in morphology and performance of native frogs induced by predation pressure from invasive mongooses
Biological Invasions (2021)
The demographic contributions of connectivity versus local dynamics to population growth of an endangered bird
Journal of Animal Ecology (2021)
Scientific Data (2021)
Biological Journal of the Linnean Society (2020)
Multifaceted implications of the competition between native and invasive crayfish: a glimmer of hope for the native’s long-term survival
Biological Invasions (2020)