Quantitative Genetics and Evolution of Head Shape in Plethodon Salamanders
Tóm tắt
The evolution of morphological diversity via selection requires that morphological traits display significant heritable genetic variation. In Plethodon salamanders, considerable evidence suggests that head shape evolves in response to selection from interspecific competition, yet the genetic underpinnings of head shape have not been quantitatively examined. Here I used geometric morphometrics and quantitative genetics to assess heritable patterns of head shape variation from hatchling salamanders in two Plethodon species (P. cinereus and P. nettingi). Head shape differed significantly between species and among clutches within species, suggesting that a sizeable proportion of head shape variation was the result of clutch effects. Further, using a full-sib animal model and restricted maximum likelihood (REML), I identified large values of maximal additive heritability for all study localities (
$$ h_{\max }^{2} > 0.65 $$
), revealing that Plethodon exhibit considerable heritable genetic variation for head shape. Comparisons of the components of heritable shape variation showed that the magnitude of shape heritability (
$$ h_{\max }^{2} $$
) did not differ among localities or species. Therefore, the potential microevolutionary shape change displayed by the two species would be similar if they were exposed to comparable selective forces. However, the direction of maximal shape heritability in morphospace differed between P. cinereus and P. nettingi, indicating that potential evolutionary shape change along these heritability trajectories would diverge between the two species. This finding implies that distinct head shapes could evolve in the two species, even if subjected to the same selection pressure. When combined with previous knowledge of patterns of head shape variation among species and ecological selection on head shape, these findings suggest that microevolutionary and macroevolutionary trends of morphological diversification in Plethodon may be explained as a result of the interaction between ecological selection and underlying patterns of genetic covariance for this multi-dimensional trait.
Tài liệu tham khảo
Adams, D. C. (1999). Methods for shape analysis of landmark data from articulated structures. Evolutionary Ecology Research, 1, 959–970.
Adams, D. C. (2000). Divergence of trophic morphology and resource use among populations of Plethodon cinereus and P. hoffmani in Pennsylvania: A possible case of character displacement. In R. C. Bruce, R. J. Jaeger, & L. D. Houck (Eds.), The biology of Plethodontid salamanders (pp. 383–394). New York: Klewer Academic/Plenum.
Adams, D. C. (2004). Character displacement via aggressive interference in Appalachian salamanders. Ecology, 85, 2664–2670.
Adams, D. C. (2007). Organization of Plethodon salamander communities: Guild-based community assembly. Ecology, 88, 1292–1299.
Adams, D. C. (2010). Parallel evolution of character displacement driven by competitive selection in terrestrial salamanders. BMC Evolutionary Biology, 10(72), 1–10.
Adams, D. C., & Church, J. O. (2008). Amphibians do not follow Bergmann’s rule. Evolution, 62, 413–420.
Adams, D. C., & Collyer, M. L. (2007). The analysis of character divergence along environmental gradients and other covariates. Evolution, 61, 510–515.
Adams, D. C., & Collyer, M. L. (2009). A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution, 63, 1143–1154.
Adams, D. C., & Nistri, A. (2010). Ontogenetic convergence and evolution of foot morphology in European cave salamanders (Family: Plethodontidae). BMC Evolutionary Biology, 10(72), 1–10.
Adams, D. C., & Rohlf, F. J. (2000). Ecological character displacement in Plethodon: Biomechanical differences found from a geometric morphometric study. Proceedings of the National Academy of Sciences, USA, 97(8), 4106–4111.
Adams, D. C., Rohlf, F. J., & Slice, D. E. (2004). Geometric morphometrics: Ten years of progress following the ‘revolution’. Italian Journal of Zoology, 71, 5–16.
Adams, D. C., West, M. E., & Collyer, M. L. (2007). Location-specific sympatric morphological divergence as a possible response to species interactions in West Virginia Plethodon salamander communities. Journal of Animal Ecology, 76, 289–295.
Anthony, C. D., Wicknick, J. A., & Jaeger, R. G. (1997). Social interactions in two sympatric salamanders: Effectiveness of a highly aggressive strategy. Behaviour, 134, 71–88.
Arif, S., Adams, D. C., & Wicknick, J. A. (2007). Bioclimatic modelling, morphology, and behaviour reveal alternative mechanisms regulating the distributions of two parapatric salamander species. Evolutionary Ecology Research, 9, 843–854.
Arnegard, M. E., McIntyre, P. B., Harmon, L. J., Zelditch, M. L., Crampton, W. G. R., Davis, J. K., et al. (2010). Sexual signal evolution outpaces ecological divergence during electric fish species radiation. American Naturalist, 176, 335–356.
Bookstein, F. L. (1991). Morphometric tools for landmark data: Geometry and biology. Cambridge: Cambridge University Press.
Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: a modeling approach for adaptive evolution. American Naturalist, 164, 683–695.
Butler, M. A., Sawyer, S. A., & Losos, J. B. (2007). Sexual dimorphism and adaptive radiation in Anolis lizards. Nature, 447, 202–205.
Collar, D. C., O’Meara, B. C., Wainwright, P. C., & Near, T. J. (2009). Piscivory limits diversification of feeding morphology in centrarchid fishes. Evolution, 63, 1557–1573.
Collar, D. C., Schulte II, J. A., O’Meara, B. C., & Losos, J. B. (2010). Habitat use affects morphological diversification in dragon lizards. Journal of Evolutionary Biology, 23, 1033–1049.
Collyer, M. L., & Adams, D. C. (2007). Analysis of two-state multivariate phenotypic change in ecological studies. Ecology, 88, 683–692.
Efimov, V. M., Kovaleva, V. Y., & Markel, A. L. (2005). A new approach to the study of genetic variability of complex characters. Heredity, 94, 101–107.
Erwin, D. H. (2007). Disparity: Morphological pattern and developmental context. Palaeontology, 50, 57–73.
Foote, M. (1997). Evolution of morphological diversity. Annual Review of Ecology and Systematics, 28, 129–152.
Gómez, J. M., Abdelaziz, M., Munoz-Pajares, J., & Perfectti, F. (2009). Heritability and genetic correlation of corolla shape and size in Erysimum mediohispanicum. Evolution, 63, 1820–1831.
Grant, P. R., & Grant, B. R. (2006). Evolution of character displacement in Darwin’s finches. Science, 313, 224–226.
Griffis, M. R., & Jaeger, R. G. (1998). Competition leads to an extinction-prone species of salamander: Interspecific territoriality in a metapopulation. Ecology, 79, 2494–2502.
Groeneveld, E., Kovac, M., & Mielenz, N. (2008). VCE user’s guide and reference manual. Version 6.0. Neustadt, Germany: Institute of Farm Animal Genetics.
Hairston, N. G. (1980). Evolution under interspecific competition: Field experiments on terrestrial salamanders. Evolution, 34, 409–420.
Harmon, L. J., Schulte, J. A., I. I., Larson, A., & Losos, J. B. (2003). Tempo and mode of evolutionary radiation in Iguanian lizards. Science, 301, 961–964.
Harmon, L. J., Losos, J. B., Davies, T. J., Gillespie, R. G., Gittleman, J. L., Jennings, W. B., et al. (2010). Early bursts of body size and shape evolution are rare in comparative data. Evolution, 64, 2385–2396.
Highton, R. (1959). The inheritance of the color phases of Plethodon cinereus. Copeia, 1959, 33–37.
Highton, R. (1960). Heritability of geographic variation in trunk segmentation in the red-backed salamander, Plethodon cinereus. Evolution, 14, 351–360.
Highton, R. (1975). Geographic variation in genetic dominance of the color morphs of the red-backed salamander, Plethodon cinereus. Genetics, 80, 363–374.
Highton, R. (1977). Comparison of microgeographic variation in morphological and electorphoretic traits. Evolutionary Biology, 10, 397–436.
Highton, R. (1995). Speciation in eastern North American salamanders of the genus Plethodon. Annual Review of Ecology and Systematics, 26, 579–600.
Hulsey, C. D., Mims, M. C., Parnell, N. F., & Streelman, J. T. (2010). Comparative rates of lower jaw diversification in cichlid adaptive radiations. Journal of Evolutionary Biology, 23, 1456–1467.
Jaeger, R. G. (1970). Potential extinction through competition between two species of terrestrial salamanders. Evolution, 24, 632–642.
Jaeger, R. G. (1971). Competitive exclusion as a factor influencing the distributions of two species of terrestrial salamanders. Ecology, 52, 632–637.
Jastrebski, C. J., & Robinson, B. W. (2004). Natural selection and the evolution of replicated trophic polymorphisms in pumpkinseed sunfish (Lepomis gibbosus). Evolutionary Ecology Research, 6, 285–305.
Kaliontzopoulou, A., Carretero, M. A., & Llorente, G. A. (2010). Intraspecific ecomorphological variation: Linear and geometric morphometrics reveal habitat-related patterns within Podarcis bocagei wall lizards. Journal of Evolutionary Biology, 23, 1234–1244.
Kelly, C. D., & Adams, D. C. (2010). Sexual selection, ontogenetic acceleration, and hypermorphosis generates male trimorphism in Wellington tree weta. Evolutionary Biology, 37, 200–209.
Klingenberg, C. P. (2003). Quantitative genetics of geometric shape: Heritability and the pitfalls of the univariate approach. Evolution, 57, 191–195.
Klingenberg, C. P., & Leamy, L. J. (2001). Quantitative genetics of geometric shape in the mouse mandible. Evolution, 55, 2342–2352.
Klingenberg, C. P., & Monteiro, L. R. (2005). Distances and directions in multidimensional shape spaces: Implications for morphometric applications. Systematic Biology, 54, 678–688.
Klingenberg, C. P., Debat, V., & Roff, D. A. (2010). Quantitative genetics of shape in cricket winge: Developmental integration in a functional structure. Evolution, 64, 2935–2951.
Lande, R. (1979). Quantitative genetic analysis of multivariate evolution, applied to brain: Body size allometry. Evolution, 33(1), 402–416.
Lande, R., & Arnold, S. J. (1983). The measurement of selection on correlated characters. Evolution, 37(6), 1210–1226.
Liebgold, E. B., Cabe, P. R., Jaeger, R. G., & Leberg, P. L. (2006). Multiple paternity in a salamander with socially monogamous behaviour. Molecular Ecology, 15, 4153–4160.
Losos, J. B. (1992). The evolution of convergent structure in Caribbean Anolis communities. Systematic Biology, 41, 403–420.
Lynch, M., & Walsh, B. (1998). Genetics and analysis of quantitative traits. Sunderland: Sinauer Associates.
Maerz, J. C., Myers, E. M., & Adams, D. C. (2006). Trophic polymorphism in a terrestrial salamander. Evolutionary Ecology Research, 8, 23–35.
Mahler, D. L., Revell, L. J., Glor, R. E., & Losos, J. B. (2010). Ecological opportunity and the rate of morphological evolution in the diversification of Greater Antillean Anoles. Evolution, 64, 2731–2745.
Marshall, J. L., Camp, C. D., & Jaeger, R. G. (2004). Potential interference competition between a patchily distributed salamander (Plethodon petraeus) and a sympatric congener (Plethodon glutinosus). Copeia, 2004, 488–495.
McPeek, M. A., Shen, L., Torrey, J. Z., & Farid, H. (2008). The tempo and mode of three-dimensional morphological evolution in male reproductive structures. American Naturalist, 171, E158–E178.
Mitteroecker, P., & Bookstein, F. L. (2008). The evolutionary role of modularity and integration in the hominid cranium. Evolution, 62(4), 943–958.
Monteiro, L. R., Diniz-Filho, J. A. F., Reis, S. F. D., & Araújo, E. D. (2002). Geometric estimates of heritability in biological shape. Evolution, 56, 563–572.
Myers, E. M., & Adams, D. C. (2008). Morphology is decoupled from interspecific competition in Plethodon salamanders in the Shenandoah Mountains. Herpetologica, 64, 281–289.
Myers, E. M., Janzen, F. J., Adams, D. C., & Tucker, J. K. (2006). Quantitative genetics of plastron shape in slider turtels (Trachemys scripta). Evolution, 60, 563–572.
O’Meara, B. C., Ane, C., Sanderson, M. J., & Wainwright, P. C. (2006). Testing for different rates of continuous trait evolution using likelihood. Evolution, 60, 922–933.
Piras, P., Colangelo, P., Adams, D. C., Buscalioni, A., Cubo, J., Kotsakis, T., et al. (2010). The Gavialis-Tomistoma debate: The contribution of skull ontogenetic allometry and growth trajectories to the study of crocodylian relationships. Evolution and Development, 12, 568–579.
Price, S. A., Wainwright, P. C., Bellwood, D. R., Kazancioglu, E., Collar, D. C., & Near, T. J. (2010). Functional innovations and morphological diversification in parrotfish. Evolution, 64, 3057–3068.
R Development Core Team. (2010). R: A language and environment for statistical computing. Version 2.12. http://cran.R-project.org. R Foundation for Statistical Computing, Vienna.
Revell, L. J. (2008). On the analysis of evolutionary change along single branches in a phylogeny. American Naturalist, 172, 140–147.
Reznick, D. N., Rodd, F. H., & Cardenas, M. (1996). Life-history evolution in guppies (Poecilia reticulata: Poecilidae). IV. Parallelism in life-history phenotypes. American Naturalist, 147, 319–338.
Roff, D. (1997). Evolutionary quantitative genetics. New York: Chapman and Hall.
Roff, D. (2000). The evolution of the G matrix: Selection or drift? Heredity, 84, 135–142.
Rohlf, F. J., & Marcus, L. F. (1993). A revolution in morphometrics. Trends in Ecology & Evolution, 8, 129–132.
Rohlf, F. J., & Slice, D. E. (1990). Extensions of the Procrustes method for the optimal superimposition of landmarks. Systematic Zoology, 39, 40–59.
Schluter, D. (2000). The ecology of adaptive radiations. Oxford: Oxford University Press.
Schluter, D., & McPhail, J. D. (1992). Ecological character displacement and speciation in sticklebacks. American Naturalist, 140, 85–108.
Sidlauskas, B. (2008). Continuous and arrested morphological diversification in sister clades of characiform fishes: A phylomorphospace approach. Evolution, 62, 3135–3156.
Simpson, G. G. (1944). Tempo and mode in evolution. New York: Columbia University Press.
Zelditch, M. L., Swiderski, D. L., Sheets, H. D., & Fink, W. L. (2004). Geometric morphometrics for biologists: A primer. Amsterdam: Elsevier/Academic Press.