The association between morphological and ecological characters across a global passerine radiation.

diet ecological characters ecological selection feeding ecology form-function morphology passerine birds selective optima

Journal

The Journal of animal ecology
ISSN: 1365-2656
Titre abrégé: J Anim Ecol
Pays: England
ID NLM: 0376574

Informations de publication

Date de publication:
04 2020
Historique:
received: 02 09 2019
accepted: 08 11 2019
pubmed: 25 12 2019
medline: 24 11 2020
entrez: 25 12 2019
Statut: ppublish

Résumé

Strong relationships between morphological and ecological characters are commonly predicted to reflect the association between form and function, with this hypothesis being well supported in restricted taxonomic and geographical contexts. Conversely, among broader sets of species, ecological variables have been shown to have limited power to explain morphological variation. To understand these apparent discrepancies, for a large and globally distributed passerine radiation, we test whether (a) the character states of four ecological variables (foraging mode, diet, strata and habitat) have different morphological optima, (b) ecological variables explain substantial variance in morphology and (c) ecological character states can be accurately predicted from morphology. We collected 10 linear morphological measurements for 782 species of corvoid passerines, and assessed (a) the fit of models of continuous trait evolution with different morphological optima for each ecological character state, (b) variation in morphological traits among ecological character states using phylogenetically corrected regressions and (c) the accuracy of morphological traits in predicting species-level membership of ecological character states using linear discriminant analysis (LDA). Models of morphological evolution with different ecological optima were well supported across numerous morphological axes, corresponding with significant differences in trait distributions among ecological character states. LDA also showed that membership of the ecological categories can be predicted with relatively high accuracy by morphology. In contrast to these findings, ecological variables explain limited amounts of variation in morphological traits. For a global radiation of passerine birds, we confirm that the generation of morphological variation is generally consistent with ecological selection pressures, but that ecological characters are of limited utility in explaining morphological differences among species. Although selection towards different optima means that membership of ecological character states tend to be well predicted by morphology, the overall morphospace of individual ecological character states tend to be broad, implying that morphology can evolve in multiple ways in response to similar selection pressures. Extensive variation in morphological adaptations among similar ecological strategies is likely to be a widespread phenomenon across the tree of life.

Identifiants

pubmed: 31873967
doi: 10.1111/1365-2656.13169
doi:

Banques de données

Dryad
['10.5061/dryad.fbg79cnr6']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1094-1108

Informations de copyright

© 2019 British Ecological Society.

Références

Alfaro, M. E., Bolnick, D. I., & Wainwright, P. C. (2005). Evolutionary consequences of many-to-one mapping of jaw morphology to mechanics in labrid fishes. The American Naturalist, 165, E140-E154. https://doi.org/10.1086/429564
Andersson, M. (1982). Female choice selects for extreme tail length in a widowbird. Nature, 299, 818-820. https://doi.org/10.1038/299818a0
Beaulieu, J. M., & O'Meara, B. (2016). OUwie: Analysis of evolutionary rates in an OU framework. R package version, 1.5.
Benkman, C. W. (1993). Adaptation to single resources and the evolution of crossbill (Loxia) diversity. Ecological Monographs, 63, 305-325. https://doi.org/10.2307/2937103
Bock, W. J. (1959). Preadaptation and multiple evolutionary pathways. Evolution, 13, 194-211. https://doi.org/10.2307/2405873
Bock, W. J. (1966). An approach to the functional analysis of the bill shape. The Auk, 83, 10-51. https://doi.org/10.2307/4082976
Bock, W. J., & Von Wahlert, G. (1965). Adaptation and the form-function complex. Evolution, 19, 269-299. https://doi.org/10.1111/j.1558-5646.1965.tb01720.x
Butler, M. A., & King, A. A. (2004). Phylogenetic comparative analysis: A modelling approach for adaptive evolution. The American Naturalist, 164, 683-695. https://doi.org/10.1086/426002
Claramunt, S., Derryberry, E. P., Remsen, J. V. Jr, & Brumfield, R. T. (2012). High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proceedings of the Royal Society B: Biological Sciences, 279, 1567-1574. https://doi.org/10.1098/rspb.2011.1922
Clavel, J., Escarguel, G., & Merceron, G. (2015). mvMORPH: An R package for fitting multivariate evolutionary models to morphometric data. Methods in Ecology and Evolution, 6, 1311-1319. https://doi.org/10.1111/2041-210x.12420
Felice, R. N., Tobias, J. A., Pigot, A. L., & Goswami, A. (2019). Dietary niche and the evolution of cranial morphology in birds. Proceedings of the Royal Society B: Biological Sciences, 286, 20182677. https://doi.org/10.1098/rspb.2018.2677
Fjeldså, J. (1982). The adaptive significance of local variations in the bill and jaw anatomy of North European red-necked grebes Podiceps grisegena. Ornis Fennica, 59, 84-98.
Frédérich, B., Sorenson, L., Santini, F., Slater, G. J., & Alfaro, M. E. (2012). Iterative ecological radiation and convergence during the evolutionary history of damselfishes (Pomacentridae). The American Naturalist, 181, 94-113.
Garland, T. Jr, Dickerman, A. W., Janis, C. M., & Jones, J. A. (1993). Phylogenetic analysis of covariance by computer simulation. Systematic Biology, 42, 265-292. https://doi.org/10.1093/sysbio/42.3.265
Gill, F. B. (1995). Ornithology. New York, NY: Macmillan.
Gillespie, R. (2004). Community assembly through adaptive radiation in Hawaiian spiders. Science, 303, 356-359. https://doi.org/10.1126/science.1091875
Hansen, T. F. (1997). Stabilizing selection and the comparative analysis of adaptation. Evolution, 51, 1341-1351. https://doi.org/10.1111/j.1558-5646.1997.tb01457.x
Harmon, L., Weir, J., Brock, C., Glor, R., & Challenger, W. (2008). GEIGER: Investigating evolutionary radiations. Bioinformatics, 24, 129-131. https://doi.org/10.1093/bioinformatics/btm538
Hutchinson, G. E. (1959). Homage to Santa Rosalia or why are there so many kinds of animals? The American Naturalist, 93, 145-159. https://doi.org/10.1086/282070
Ives, A. R. (2018). R2s for correlated data: Phylogenetic models, LMMs, and GLMMs. Systematic Biology, 68, 234-251. https://doi.org/10.1093/sysbio/syy060
Ives, A. R., & Li, D. (2018). rr2: An R package to calculate R2s for regression models. The Journal of Open Source Software, 3, 1028. https://doi.org/10.21105/joss.01028
Jønsson, K. A., Borregaard, M. K., Carstensen, D. W., Hansen, L. A., Kennedy, J. D., Machac, A., … Rahbek, C. (2017). Biogeography and biotic assembly of Indo-Pacific corvoid passerine birds. Annual Review of Ecology, Evolution, and Systematics, 48, 231-253. https://doi.org/10.1146/annurev-ecolsys-110316-022813
Jønsson, K. A., Fabre, P.-H., Fritz, S. A., Etienne, R. S., Ricklefs, R. E., Jorgensen, T. B., … Irestedt, M. (2012). Ecological and evolutionary determinants for the adaptive radiation of the Madagascan vangas. Proceedings of the National Academy of Sciences of the United States of America, 109, 6620-6625. https://doi.org/10.1073/pnas.1115835109
Jønsson, K. A., Fabre, P. H., Kennedy, J. D., Holt, B. G., Borregaard, M. K., Rahbek, C., & Fjeldså, J. (2016). A supermatrix phylogeny of corvoid passerine birds (Aves: Corvides). Molecular Phylogenetics and Evolution, 94, 87-94. https://doi.org/10.1016/j.ympev.2015.08.020
Jønsson, K. A., Fabre, P. H., Ricklefs, R. E., & Fjeldså, J. (2011). Major global radiation of corvoid birds originated in the proto-Papuan archipelago. Proceedings of the National Academy of Sciences of the United States of America, 108, 2328-2333. https://doi.org/10.1073/pnas.1018956108
Kennedy, J. (2019). Data from: The associl characters across a global passerine radiation, v2, Dryad, Dataset. https://datadryad.org/stash/dataset/doi:10.5061/dryad.fbg79cnr6
Kennedy, J. D., Borregaard, M. K., Jønsson, K. A., Marki, P. Z., Fjeldså, J., & Rahbek, C. (2016). The influence of wing morphology upon the dispersal, geographical distributions and diversification of the Corvides (Aves; Passeriformes). Proceedings of the Royal Society B: Biological Sciences, 283, 20161922. https://doi.org/10.1098/rspb.2016.1922
Kennedy, J. D., Borregaard, M. K., Marki, P. Z., Machac, A., Fjeldså, J., & Rahbek, C. (2018). Expansion in geographical and morphological space drives continued lineage diversification in a global passerine radiation. Proceedings of the Royal Society B: Biological Sciences, 285, 20182181. https://doi.org/10.1098/rspb.2018.2181
Kennedy, J. D., Weir, J. T., Hooper, D. M., Tietze, D. T., Martens, J., & Price, T. D. (2012). Ecological limits on diversification of the Himalayan core Corvoidea. Evolution, 66, 2599-2613. https://doi.org/10.1111/j.1558-5646.2012.01618.x
Kuhn, T. S., Mooers, A. Ø., & Thomas, G. H. (2011). A simple polytomy resolver for dated phylogenies. Methods in Ecology and Evolution, 2, 427-436. https://doi.org/10.1111/j.2041-210X.2011.00103.x
Lack, D. (1947). Darwin's finches. Cambridge: Cambridge University Press.
Lande, R. (1976). Natural selection and random genetic drift in phenotypic evolution. Evolution, 30, 314-334.
Lapiedra, O., Sol, D., Carranza, S., & Beaulieu, J. M. (2013). Behavioural changes and the adaptive diversification of pigeons and doves. Proceedings of the Royal Society B: Biological Sciences, 280, 20122893. https://doi.org/10.1098/rspb.2012.2893
Leisler, B., Ley, H. W., & Winkler, H. (1989). Habitat, behaviour and morphology of Acrocephalus warblers: An integrated analysis. Ornis Scandinavica, 20, 181-186. https://doi.org/10.2307/3676911
Leisler, B., & Winkler, H. (2003). Morphological consequences of migration in passerines. In P. Berthold, E. Gwinner, & E. Sonnenschein (Eds.), Avian migration (pp. 175-186). Berlin, Heidelberg: Springer.
Losos, J. B. (1990a). The evolution of form and function: Morphology and locomotor performance in West Indian Anolis lizards. Evolution, 44, 1189-1203. https://doi.org/10.1111/j.1558-5646.1990.tb05225.x
Losos, J. B. (1990b). Ecomorphology, performance capability, and scaling of West Indian Anolis lizards: An evolutionary analysis. Ecological Monographs, 60, 369-388. https://doi.org/10.2307/1943062
Losos, J. B., & Sinervo, B. (1989). The effects of morphology and perch diameter on sprint performance of Anolis lizards. Journal of Experimental Biology, 145, 23-30.
MacArthur, R. H. (1958). Population ecology of some warblers of northeastern coniferous forests. Ecology, 39, 599-619. https://doi.org/10.2307/1931600
Mahler, D. L., Ingram, T., Revell, L. J., & Losos, J. B. (2013). Exceptional convergence on the macroevolutionary landscape in island lizard radiations. Science, 341, 292-295. https://doi.org/10.1126/science.1232392
Marchetti, K., Price, T., & Richman, A. (1995). Correlates of wing morphology with foraging behaviour and migration distance in the genus Phylloscopus. Journal of Avian Biology, 26, 177-181. https://doi.org/10.2307/3677316
Marki, P. Z. M., Kennedy, J. D., Cooney, C., Rahbek, C., & Fjeldså, J. (2019). Adaptive radiation and the evolution of nectarivory in a large songbird clade. Evolution, 73, 1226-1240. https://doi.org/10.1111/evo.13734
Miles, D. B., & Ricklefs, R. E. (1984). The correlation between ecology and morphology in deciduous forest passerine birds. Ecology, 65, 1629-1640. https://doi.org/10.2307/1939141
Miles, D. B., Ricklefs, R. E., & Travis, J. (1987). Concordance of ecomorphological relationships in three assemblages of passerine birds. The American Naturalist, 129, 347-364. https://doi.org/10.1086/284641
Muschick, M., Indermaur, A., & Salzburger, W. (2012). Convergent evolution within an adaptive radiation of cichlid fishes. Current Biology, 22, 2362-2368. https://doi.org/10.1016/j.cub.2012.10.048
Navalón, G., Bright, J. A., Marugán-Lobón, J., & Rayfield, E. J. (2019). The evolutionary relationship among beak shape, mechanical advantage, and feeding ecology in modern birds. Evolution, 73, 422-435. https://doi.org/10.1111/evo.13655
Norberg, U. M. (1979). Morphology of the wings, legs and tail of three coniferous forest tits, the goldcrest, and the treecreeper in relation to locomotor pattern and feeding station selection. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 287, 131-165. https://doi.org/10.1098/rstb.1979.0054
Partridge, L. (1976). Some aspects of the morphology of Blue tits (Parus caemleus) and Coal tits (Parus ater) in relation to their behaviour. Journal of Zoology, 179, 121-133. https://doi.org/10.1111/j.1469-7998.1976.tb03230.x
Pearson, R. (2016). GoodmanKruskal: Association analysis for categorical variables. R package version 0.0.2. Retrieved from https://CRAN.R-project.org/package=GoodmanKruskal
Pigot, A. L., & Tobias, J. A. (2013). Species interactions constrain geographic range expansion over evolutionary time. Ecology Letters, 16, 330-338. https://doi.org/10.1111/ele.12043
Pigot, A. L., Trisos, C. H., & Tobias, J. A. (2016). Functional traits reveal the expansion and packing of ecological niche space underlying an elevational diversity gradient in passerine birds. Proceedings of the Royal Society B: Biological Sciences, 283, 20152013. https://doi.org/10.1098/rspb.2015.2013
Price, T. (2008). Speciation in birds. Eckert, CO: Roberts and Company.
Rabosky, D. L. (2015). No substitute for real data: A cautionary note on the use of phylogenies from birth-death polytomy resolvers for downstream comparative analyses. Evolution, 69, 3207-3216. https://doi.org/10.1111/evo.12817
Rabosky, D. L., Santini, F., Eastman, J., Smith, S. A., Sidlauskas, B., Chang, J., & Alfaro, M. E. (2013). Rates of speciation and morphological evolution are correlated across the largest vertebrate radiation. Nature Communications, 4, 1958. https://doi.org/10.1038/ncomms2958
Remsen, J. V. Jr, & Robinson, S. K. (1990). A classification scheme for foraging behavior of birds in terrestrial habitats. Studies in Avian Biology, 13, 144-160.
Revell, L. J. (2009). Size-correction and principal components for interspecific comparative studies. Evolution, 63, 3258-3268. https://doi.org/10.1111/j.1558-5646.2009.00804.x
Revell, L. J. (2012). phytools: An R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3, 217-223. https://doi.org/10.1111/j.2041-210X.2011.00169.x
Richman, A. D., & Price, T. (1992). Evolution of ecological differences in the Old World leaf warblers. Nature, 355, 817-821. https://doi.org/10.1038/355817a0
Ricklefs, R. E. (1987). Community diversity: Relative roles of local and regional processes. Science, 235, 167-171. https://doi.org/10.1126/science.235.4785.167
Ricklefs, R. E. (2005). Small clades at the periphery of passerine morphological space. The American Naturalist, 165, 651-659. https://doi.org/10.1086/429676
Ricklefs, R. E. (2012). Species richness and morphological diversity of passerine birds. Proceedings of the National Academy of Sciences of the United States of America, 109, 14482-14487. https://doi.org/10.1073/pnas.1212079109
Ricklefs, R. E., & Miles, D. B. (1994). Ecological and evolutionary inferences from morphology: An ecological perspective. In P. C. Wainwright & S. M. Reilly (Eds.), Ecological morphology: Integrative organismal biology (pp. 13-41). Chicago, IL: The University of Chicago Press.
Ricklefs, R. E., & Travis, J. (1980). A morphological approach to the study of avian community organization. The Auk, 97, 321-338.
Robinson, S. K., & Holmes, R. T. (1982). Foraging behavior of forest birds: The relationships among search tactics, diet, and habitat structure. Ecology, 63, 1918-1931. https://doi.org/10.2307/1940130
Schluter, D. (2000). The ecology of adaptive radiation. Oxford: Oxford University Press.
Schluter, D., & Grant, P. R. (1984a). Determinants of morphological patterns in communities of Darwin's finches. The American Naturalist, 123, 175-196. https://doi.org/10.1086/284196
Schluter, D., & Grant, P. R. (1984b). Ecological correlates of morphological evolution in a Darwin's finch, Geospiza difficilis. Evolution, 38, 856-869. https://doi.org/10.1111/j.1558-5646.1984.tb00357.x
Schoener, T. W. (1974). Resource partitioning in ecological communities. Science, 185, 27-39. https://doi.org/10.1126/science.185.4145.27
Suhonen, J., Alatalo, R. V., & Gustafsson, L. (1994). Evolution of foraging ecology in Fennoscandian tits (Parus spp.). Proceedings of the Royal Society of London. Series B: Biological Sciences, 258, 127-131. https://doi.org/10.1098/rspb.1994.0152
Tokita, M., Yano, W., James, H. F., & Abzhanov, A. (2017). Cranial shape evolution in adaptive radiations of birds: Comparative morphometrics of Darwin's finches and Hawaiian honeycreepers. Philosophical Transactions of the Royal Society B: Biological Sciences, 372, 20150481.
Toro, E., Herrel, A., & Irschick, D. (2004). The evolution of jumping performance in Caribbean Anolis lizards: Solutions to biomechanical trade-offs. The American Naturalist, 163, 844-856.
Uyeda, J. C., Caetano, D. S., & Pennell, M. W. (2015). Comparative analysis of principal components can be misleading. Systematic Biology, 64, 677-689. https://doi.org/10.1093/sysbio/syv019
Van Buskirk, J., McCollum, S. A., & Werner, E. E. (1997). Natural selection for environmentally induced phenotypes in tadpoles. Evolution, 51, 1983-1992. https://doi.org/10.2307/2411018
Wainwright, P. C., Alfaro, M. E., Bolnick, D. I., & Hulsey, C. D. (2005). Many-to-one mapping of form to function: A general principle in organismal design? Integrative and Comparative Biology, 45, 256-262. https://doi.org/10.1093/icb/45.2.256
White, A. E. (2016). Geographical barriers and dispersal propensity interact to limit range expansions of himalayan birds. The American Naturalist, 188, 99-112. https://doi.org/10.1086/686890
Wilman, H., Belmaker, J., Simpson, J., de la Rosa, C., Rivadeneira, M. M., & Jetz, W. (2014). EltonTraits 1.0: Species-level foraging attributes of the world's birds and mammals: Ecological Archives E095-178. Ecology, 95, 2027-2027.
Wilson, D. S. (1975). The adequacy of body size as a niche difference. The American Naturalist, 109, 769-784. https://doi.org/10.1086/283042
Winkler, H., & Leisler, B. (1985). Morphological aspects of habitat selection in birds. In M. Cody (Ed.), Habitat selection in birds (pp. 415-434). New York: Academic Press.

Auteurs

Jonathan D Kennedy (JD)

Department of Animal and Plant Sciences, University of Sheffield, Sheffield, UK.

Petter Z Marki (PZ)

Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
Natural History Museum, University of Oslo, Oslo, Norway.

Jon Fjeldså (J)

Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark.

Carsten Rahbek (C)

Center for Macroecology, Evolution and Climate, GLOBE Institute, University of Copenhagen, Copenhagen, Denmark.
Department of Life Sciences, Imperial College London, Ascot, UK.
Danish Institute for Advanced Study, University of Southern Denmark, Odense, Denmark.

Articles similaires

Genome, Chloroplast Phylogeny Genetic Markers Base Composition High-Throughput Nucleotide Sequencing
Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice

Classifications MeSH