University of South Florida
Scholar Commons
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Mega-Evolutionary Dynamics of the Adaptive
Radiation of Birds
Christopher R. Cooney
University of Sheeld
Jen A. Bright
University of South Florida0'(7/-.9:8,+*:
Elliot J. R. Capp
University of Sheeld
Angela M. Chira
University of Sheeld
Emma C. Hughes
University of Sheeld
See next page for additional authors
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Mega-evolutionary dynamics of the adaptive radiation of birds
Christopher R. Cooney
#1
, Jen A. Bright
#1,2,3
, Elliot J. R. Capp
1
, Angela M. Chira
1
, Emma C.
Hughes
1
, Christopher J. A. Moody
1
, Lara O. Nouri
1
, Zoë K. Varley
1
, and Gavin H.
Thomas
1,4,*
1
Department of Animal and Plant Sciences, University of Sheffield, Sheffield, S10 2TN, UK
2
School of Geosciences, University of South Florida, Tampa, FL 33620, USA
3
Center for Virtualization and Applied Spatial Technologies, University of South Florida, Tampa,
FL 33620, USA
4
Bird Group, Department of Life Sciences, The Natural History Museum, Tring, Hertfordshire, UK
#
These authors contributed equally to this work.
Abstract
The origin and expansion of biological diversity is regulated by both developmental trajectories1,2
and limits on available ecological niches3–7. As lineages diversify an early, often rapid, phase of
species and trait proliferation gives way to evolutionary slowdowns as new species pack into ever
more densely occupied regions of ecological niche space6,8. Small clades such as Darwin’s
finches demonstrate that natural selection is the driving force of adaptive radiations, but how
microevolutionary processes scale up to shape the expansion of phenotypic diversity over much
longer evolutionary timescales is unclear9. Here we address this problem on a global scale by
analysing a novel crowd-sourced dataset of 3D-scanned bill morphology from >2000 species. We
find that bill diversity expanded early in extant avian evolutionary history before transitioning to a
phase dominated by morphospace packing. However, this early phenotypic diversification is
decoupled from temporal variation in evolutionary rate: rates of bill evolution vary among lineages
but are comparatively stable through time. We find that rare but major discontinuities in phenotype
emerge from rapid increases in rate along single branches, sometimes leading to depauperate
clades with unusual bill morphologies. Despite these jumps between groups, the major axes of
within-group bill shape evolution are remarkably consistent across birds. We reveal that
macroevolutionary processes underlying global-scale adaptive radiations support Darwinian9 and
Simpsonian4 ideas of microevolution within adaptive zones and accelerated evolution between
distinct adaptive peaks.
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*
author for correspondence: gavin.thomas@sheffield.ac.uk.
Contributions
Christopher R. Cooney, Jen A. Bright, and Gavin H. Thomas conceived of the study, designed analytical protocols, analysed the data
and wrote the manuscript. All authors collected and processed data and provided editorial input into the manuscript.
Competing financial interests. None.
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Published in final edited form as:
Nature
. 2017 February 16; 542(7641): 344–347. doi:10.1038/nature21074.
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The role of adaptive radiations as the source of much of the world’s biological diversity has
been widely emphasised10,11. Studies of small clades have provided insights into the role of
natural selection as a diversifying force, but cannot illuminate the processes that shape the
diversity and discontinuities of radiations over much longer evolutionary timeframes.
Indeed, at large taxonomic scales, the diversification of clades11,12 and traits13 shows no
evidence of the predicted slowdowns in evolutionary rates, despite there being numerous
examples in small clades3,14–16. This apparent paradox is potentially resolved by G. G.
Simpson’s model, in which major jumps to new adaptive zones (“quantum evolution”) can
occur unpredictably throughout clade history. These jumps give rise to rapid lineage
expansion into previously unoccupied niche space as sub-clades continue to radiate within
distinct adaptive zones and subzones4. Simpson’s models introduced the concept of ‘mega-
evolution’—diversification over large temporal and spatial scales—unifying microevolution
with other factors such as ecological opportunity and evolutionary constraints that shape the
macroevolutionary trajectories of radiating lineages. However, while phylogenetic studies
involving thousands of species have demonstrated heterogeneity in rates of phenotypic
evolution13,17, it is unclear whether the processes outlined by Simpson play an important
role in large-scale adaptive radiations. This is because previous studies have been unable to
specifically assess the macroevolutionary dynamics of ecologically relevant traits. Here we
study the evolution of an important ecological trait (bill shape) across an entire Class of
organisms (birds) to elucidate the processes shaping the accumulation of phenotypic
diversity within a global-scale adaptive radiation.
Our approach is based around a novel data set describing avian bill shape. The avian bill is
closely associated with species’ dietary and foraging niches16,18,19 and represents a highly-
adaptable ecological trait known to play a key role in classic avian adaptive
radiations16,18,20. We took 3D scans of museum study skins comprising >2000 species
(>97% of extant genera) representing the full range of bill shape diversity. We landmarked
bills (Extended Data Fig. 1) using a bespoke crowd-sourcing website, www.markmybird.org,
and quantified the bill shape morphospace of extant birds using Procrustes superimposition
and Principal Components Analyses (PCA, see Methods). The first eight PC axes explain
>99% of the total variation in bill shape (Fig. 1). PC1 (58% of overall shape variation)
describes the volumetric aspect ratio from elongated (e.g. sword-billed hummingbird,
Ensifera ensifera
) to stout bills (e.g. large ground finch,
Geospiza magnirostris
) and captures
the range of shape variation encompassed by standard linear measurements (length, width
and depth). Variation in these bill dimensions may relate to fine scale division of the dietary
or foraging niche among closely related species, but cannot explain the diversity of shapes
observed among extant birds. More complex aspects of shape (42% of total variation) are
explained by the remaining PCs (Fig. 1), which retain high phylogenetic signal (Extended
Data Table 1). Importantly, although these higher shape axes explain a low proportion of
shape variance, they capture large differences in ecologically relevant aspects of bill shape.
The narrow (long tail) distributions of higher shape axes, compared to the broad distribution
of PC1 (Extended Data Fig. 2, Extended Data Table 1), suggest that the majority of species
have relatively simple bill shapes and diversify in densely packed regions of bill
morphospace.
Cooney et al. Page 2
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We tested an important prediction of Simpson’s model by evaluating how niche expansion
and niche packing have contributed to the accumulation of bill shape disparity throughout
avian evolutionary history. We estimated multivariate disparity through time using ancestral
state estimates derived from rate heterogeneous models of trait evolution (see Methods)13.
In 1 million year time slices, we calculated disparity as the sum of the variances21 from the
first eight shape axes. We compared observed disparity through time with two null models—
constant-rate (Brownian motion) and rate heterogeneous trait evolution—that are unbiased
with respect to niche filling processes (see Methods). Relative to these null expectations, we
find that the filling of avian bill morphospace through time shows a striking dominance of
niche expansion early in avian history, followed by a more recent transition towards niche
packing (Fig. 2a-b, Extended Data Fig. 2). Our data includes only extant taxa due to the poor
preservation of bills in the avian fossil record22, although we acknowledge that some extinct
taxa had bills that may lie outside the range of extant diversity (e.g. Phorusrhacidae,
Gastornithidae, Dromornithidae). This can result in underestimates of disparity particularly
if these morphologies arise early in clade history22–24. Our analyses are therefore
conservative with respect to transitions from bill morphospace expansion to filling and
consistent with recent studies of avian skeletal material22. The transition in the mode of
niche filling is consistent with a process of ever-finer divisions of niche space and would be
expected to correspond to slowdowns in rates of bill evolution. However, the switch from
niche expansion to niche packing does not map onto temporal trends in the rate of bill shape
evolution. Plotting evolutionary rates through time reveals an initial low rate followed by a
moderate (two to four-fold) increase that is coincident with the divergence of many non-
Passerine orders (Fig. 2c, Extended Data Fig. 3, 4). Thereafter average rates dip and then
rise gradually with less than 1.5-fold total variation over ~80 million years of evolutionary
history, contrasting sharply with >250-fold variation in evolutionary rate among individual
lineages (Fig. 3).
The disjunction between rates of evolution and the accumulation of bill shape disparity
suggests that temporal trends in evolutionary rate are not necessarily indicative of the
underlying mode of niche filling. This decoupling could arise if some clades diverge rapidly
within regions of morphospace that are occupied by other clades, but where the respective
clades occur in allopatry. To test this idea, we mapped rates of bill evolution onto the avian
phylogeny (Fig. 3, Extended Data Fig. 3-5). We find several instances of clades exhibiting
exceptionally high rates of evolution consistent with speciational or phyletic evolution
within adaptive subzones (Fig. 3). Some of the fastest rates of bill evolution arise in island
radiations of passerine birds, where ecological divergence has been closely linked to
ecological opportunity (e.g. Malagasy vangas16, Galapagos finches18, Hawaiian
honeycreepers20), suggesting that lineages radiating on isolated island archipelagos can
explore morphological space independently of the global avifauna. Notably high rates of bill
evolution occur in several large species-rich clades that have high speciation rates, including
the Psittaciformes, the Furnariidae, and the Passeroidea. However, these clades occupy
regions of morphospace that overlap with other more slowly evolving clades and so, while
rapid divergence among close relatives within a subzone leads to locally high rates, they do
not contribute uniquely to the global expansion of morphospace. In contrast, some large
Cooney et al. Page 3
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