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Macroevolutionary convergence connects morphological form to ecological function in birds

Nature Ecology & Evolution volume 4, pages 230–239 (2020)Cite this article

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Abstract

Animals have diversified into a bewildering variety of morphological forms exploiting a complex configuration of trophic niches. Their morphological diversity is widely used as an index of ecosystem function, but the extent to which animal traits predict trophic niches and associated ecological processes is unclear. Here we use the measurements of nine key morphological traits for >99% bird species to show that avian trophic diversity is described by a trait space with four dimensions. The position of species within this space maps with 70–85% accuracy onto major niche axes, including trophic level, dietary resource type and finer-scale variation in foraging behaviour. Phylogenetic analyses reveal that these form–function associations reflect convergence towards predictable trait combinations, indicating that morphological variation is organized into a limited set of dimensions by evolutionary adaptation. Our results establish the minimum dimensionality required for avian functional traits to predict subtle variation in trophic niches and provide a global framework for exploring the origin, function and conservation of bird diversity.

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Fig. 1: The avian morphospace.
Fig. 2: Trophic structuring of multidimensional morphospace.
Fig. 3: Partitioning of avian morphospace across trophic levels and niches.
Fig. 4: Scale and context of macroevolutionary convergence in birds.
Fig. 5: Convergent evolutionary trajectories through avian morphospace.
Fig. 6: The global mapping of form to function across birds.

Data availability

All geographical and phylogenetic data are publicly available from www.birdlife.org and www.birdtree.org, respectively. Morphological data and ecological niche assignments are provided in Supplementary Dataset 1.

Code availability

The code to conduct the analyses is available on request from the authors.

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Acknowledgements

We thank numerous field biologists and explorers who collected and prepared the specimens used in this study. We thank the Natural History Museum, the American Museum of Natural History and 63 other research collections for providing access to specimens. Illustrations are reproduced with permission of Lynx Edicions. Financial support was received from a Royal Society University Research Fellowship (A.L.P.); a PhD studentship funded by the University of Oxford Clarendon Fund and the US–UK Fulbright Commission (C.S.); and Natural Environment Research Council grant nos. NE/I028068/1 and NE/P004512/1 (J.A.T.). Secondary sources of funding are listed in the Supplementary Information, along with a complete list of individuals and institutions that contributed directly to data collection, logistics and specimen access.

Author information

Author notes

  1. These authors contributed equally: Alex L. Pigot, Catherine Sheard.

Authors and Affiliations

  1. Centre for Biodiversity and Environment Research, Department of Genetics, Evolution and Environment, University College London, London, UK

    Alex L. Pigot

  2. Department of Zoology, University of Oxford, Oxford, UK

    Alex L. Pigot, Catherine Sheard, Tom P. Bregman, Uri Roll, Nathalie Seddon, Christopher H. Trisos & Joseph A. Tobias

  3. School of Biology, University of St Andrews, St Andrews, UK

    Catherine Sheard

  4. Cornell Lab of Ornithology, Ithaca, NY, USA

    Eliot T. Miller

  5. Department of Biological Sciences, University of Idaho, Moscow, ID, USA

    Eliot T. Miller

  6. Future-Fit Foundation, London, UK

    Tom P. Bregman

  7. Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada

    Benjamin G. Freeman

  8. Mitrani Department of Desert Ecology, Jacob Balaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Beer-Sheva, Israel

    Uri Roll

  9. African Climate and Development Initiative, University of Cape Town, Cape Town, South Africa

    Christopher H. Trisos

  10. School for Environment and Sustainability, University of Michigan, Ann Arbor, MI, USA

    Brian C. Weeks

  11. Department of Ornithology, American Museum of Natural History, New York, NY, USA

    Brian C. Weeks

  12. Department of Life Sciences, Imperial College London Silwood Park, Ascot, UK

    Joseph A. Tobias

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  1. Alex L. Pigot
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Contributions

J.A.T. and A.L.P. conceived and coordinated the study. J.A.T., A.L.P., C.S., E.T.M. and U.R. designed the study. C.S., A.L.P., T.P.B., B.G.F., U.R., C.H.T., B.C.W., N.S. and J.A.T. compiled the morphological, ecological and geographical data. A.L.P. led the analyses. All authors contributed to the writing of the manuscript.

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Correspondence to Alex L. Pigot or Joseph A. Tobias.

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Extended data

Extended Data Fig. 1 Diagram of linear measurements of avian morphology.

a, Resident frugivorous tropical passerine (fiery-capped manakin, Machaeropterus pyrocephalus) showing four beak measurements: (1) beak length measured from tip to skull along the culmen; (2) beak length measured from the tip to the anterior edge of the nares; (3) beak depth; (4) beak width. b, Insectivorous migratory temperate-zone passerine (redwing, Turdus iliacus) showing five body measurements: (5) tarsus length; (6) wing length from carpal joint to wingtip; (7) secondary length from carpal joint to tip of the outermost secondary; (8) Kipp’s distance, calculated as wing length minus first-secondary length; (9) tail length. Analyses exclude Kipp’s distance, and thus include 8 traits shown here (plus body mass, making 9 traits in total). Illustration by Richard Johnson.

Extended Data Fig. 2 Repeatability of avian morphological trait measurements.

Data points show replicate measurements taken by different researchers on the same museum specimens for a subset of our global dataset (n = 2752 specimens of n = 2523 species). Points falling along the 1:1 line indicate a perfect correspondence between measurers. The % of total trait variance (Var) occurring between measurers within specimens is shown. The number of specimens varies across traits and is indicated in the top left of each plot.

Extended Data Fig. 3 Trait loadings along principal component (PC) dimensions based on all 9 phenotypic traits.

Results are shown for PC axes representing variation in shape, and thereby excluding PC1 which represents variation in body size. Colours indicate the increasing density of species (from yellow to red) on each 2-dimensional plane (n =9,963 species). See Supplementary Table 3 for trait loadings.

Extended Data Fig. 4 Density profiles through multidimensional morphospace.

The relative density of species with distance from the centroid of nine-dimensional morphospace is calculated for concentric shells of 1-unit diameter. Density is shown for all species (n = 9,963) and each trophic niche separately.

Extended Data Fig. 5 Avian trophic niches and foraging niches.

Silhouettes depict archetypal species belonging to (a) nine specialist trophic niches, (b) seven major foraging niches used by terrestrial invertivores, and (c) six major foraging niches used by aquatic predators. Foraging niches for the remaining seven specialist trophic niches are less diverse and are not shown. See Supplementary Table 4 for a full list and description of trophic and foraging niches. Bird silhouettes were generated directly from published illustrations with permission of Lynx Edicions (https://www.hbw.com/) or downloaded from online repositories without restrictions on use: http://phylopic.org/image/6da653ca-1baa-4852-b9db-aff15404cbf7/ http://www.clker.com/cliparts/f/7/9/a/11949848182045168189eagle_01.svg.med.png http://phylopic.org/image/05cd7d8c-6b2c-4b97-b7b8-053559019eeb/.

Extended Data Fig. 6 Classification accuracy (%) using alternative classification algorithms.

Predictions of species trophic levels, trophic niches and foraging niches using (a) Random Forest, (b) Mixture Discriminant Analysis, and (c) Linear Discriminant Analysis for all birds (n = 9,963 species) on the basis of body size (mass), size and beak traits, or the full nine-dimensional morphospace. Stippling indicates improvement in predictive accuracy after omitting omnivores and foraging generalists (see Methods).

Extended Data Fig. 7 Intermediate dimensionality of avian niche space.

Accuracy curves indicate the maximum predictability of (a-b) trophic and (c) foraging niches in morphospaces consisting of different numbers of trait dimensions. Results are shown for a morphospace based on (a,c) standard and (b) phylogenetic principal components analysis. Accuracy is shown for individual niches (colours matching those depicted in Fig. 3) and total niche space (black, DTotal). Points indicate the level of niche dimensionality (D) according to Levene’s index. Horizontal bar shows the mean \(\left( {\bar D} \right)\) and range in dimensionality estimates for each niche.

Extended Data Fig. 8 The dimensionality of avian trophic and foraging niches.

a-b, The identity of the trait dimensions best describing (a) trophic and (b) foraging niches for different levels of dimensionality. c-d, estimates of dimensionality (D) according to Levene’s index for (c) trophic niches and (d) foraging niches. Each niche is given separately, and with all niches combined (‘All’), along with the identity of the principal component (PC) dimensions (coloured squares) that best predict the niche.

Extended Data Fig. 9 Non-random trait packing within avian trophic niches.

a, Phylogenetic distribution of avian trophic niches across the complete avian tree (n = 9,963 species) with species lacking genetic data inserted according to taxonomic constraints41. Tips and internal branches connected by species sharing the same trophic niche are highlighted across the avian evolutionary tree. b, Mean pairwise trait distance between species in each trophic niche (points) is less than expected due to phylogenetic relatedness, based on species with both morphological and genetic data (n = 6,666). Box and whiskers show 50% interquartile range and 95% confidence interval of mean pairwise trait distances expected under an evolutionary null model. This null model incorporates a multi-rate process of Brownian trait evolution whereby rates of evolution can vary both across lineages and over time. Bird silhouettes were generated directly from published illustrations with permission of Lynx Edicions (https://www.hbw.com/) or downloaded from online repositories without restrictions on use: http://phylopic.org/image/6da653ca-1baa-4852-b9db-aff15404cbf7/ http://www.clker.com/cliparts/f/7/9/a/11949848182045168189eagle_01.svg.med.png http://phylopic.org/image/05cd7d8c-6b2c-4b97-b7b8-053559019eeb/.

Extended Data Fig. 10 The distance across morphospace independently evolved by phenotypically matched pairs of avian families.

We calculated the average phenotypic distance evolved by each clade since they last shared a common ancestor with their phenotypically matched family (n = 91 pairs). Distances are expressed in (a) raw morphological units (trait axes scaled to unit variance) and (b) as a proportion of the total span of morphospace. On average, each clade within a matched family pair has independently evolved a distance equivalent to one-third of the total span of morphospace. For comparison, the 9 matched family pairs that are also sister clades (that is each other’s closest relative) have each on average evolved a distance equivalent to only ~10% of the total span of morphospace. Position of letters indicate the average distance evolved by families within sister clades: (A) Cettiidae-Phylloscopidae, (B) Cardinalidae-Thraupidae, (C) Emberizidae-Passerellidae, (D) Phalacrocoracidae-Sulidae, (E) Odontophoridae-Phasianidae, (F) Strigidae-Tytonidae, (G) Ardeidae-Threskiornithidae, (H) Cacatuidae-Psittacidae, (I) Accipitridae-Cathartidae.

Supplementary information

Supplementary Information

Supplementary Methods, Tables 1–4, Figs. 1–6, acknowledgements and references.

Reporting Summary

Supplementary Dataset 1

Supplementary Database 1: Species morphological PC scores and ecological niche assignments (n = 9,963 species).

Supplementary Dataset 2

Supplementary Database 2: Phenotypically matched family pairs (n = 91 pairs), along with their diet, divergence time, geographic and foraging niche overlap.

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Pigot, A.L., Sheard, C., Miller, E.T. et al. Macroevolutionary convergence connects morphological form to ecological function in birds. Nat Ecol Evol 4, 230–239 (2020). https://doi.org/10.1038/s41559-019-1070-4

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