Thread by @GNavalon

Very excited to see our work published in @Nature! We present 1 of the most comprehensive characterisations of 3D #shape across (almost) the whole #skeleton in a group of land #vertebrates. Paper: nature.com/articles/s4158…

We studied the diversification of skeletal forms during the radiation that originated the staggering diversity of living #birds. Bird pics by @fieldpalaeo! Collage by moi

Our work harkens back to some of the most fundamental early works on macroevo. theory by George G. Simpson. Among the most influential palaeos of all times, & one of the main reasons palaeontology as a discipline made it into the high table of the Modern Evolutionary Synthesis.

He suggested in one of the foundational works of macroevo. theory that most adaptive radiations undergo a mode of evolution characterised by 2 features:
1.Early expansion of ecologies and morphological disparity.
2.Early partitioning of that ecological and morphological space.

Crown birds are one of the most important groups of land vertebrates which underwent a large-scale radiation after the K-Pg extinction that decimated terrestrial faunas including non-avian dinosaurs (also no stem-bird groups made it!). Art: Phillip Krzeminski.

Birds seem to have recovered fairly quick from the catastrophe: fossils from living groups (e.g., mousebirds, frigatebirds, penguins) can be recognised as early as the Paleocene, only a few million years after the extinction event.

These fossils have been used to calibrate the timing of splitting events in avian phylogeny also suggesting a whole lot of cladogenesis occurred in the first million years of the Cenozoic era.

Super-speciose clades of predominantly water-linked and terrestrial/arboreal birds split back then, suggesting that partitioning of ecological space occurred early in the wake of the mass extinction. Pics @fieldpalaeo

Crucial earlier work (Saupe et al., 2019) in niche modelling suggests that the ecological niches in many of these groups of birds might have been acquired early and retained during the whole Cenozoic.

But what about morphology? Did it follow ecological patterns?

The short answer is we mostly don’t know. A slightly longer answer is that most our evidence comes from studies of the skull that seemingly suggest that, at least, beak shapes experienced an early expansion of morphologies. Redrawn from Cooney et al., 2017.

However, evolution acts upon the whole organism, and individual parts do not necessarily represent the whole (mosaic evolution). By studying the evolution of the morphology across the whole skeleton we could provide some long-awaited answers.

While we found evidence for an early expansion of skeletal forms in the aftermath of the K-Pg extinction and also for some localised regions , like the shape of beaks (confirming previous results!), early partitioning of these forms is, however, generally rare!

So, it seems that the patterns look a bit more like this:

Lineages ‘jumped’ between adaptive zones multiple times during later events throughout the Cenozoic. One of the main exceptions to this pattern is the early establishment of different skeletal forms in non-passerine landbirds.

This likely means that after an initial differentiation of skeletal morphotypes in landbirds, subsequent evolution mostly affected lower-scale aspects of their skeletal anatomy (e.g., finger orientation). In short, parrots mostly stayed parrots, eagles mostly stayed eagles.

This contrasts with their sister clade ‘waterbirds’ which continually re-explored a limited set of skeletal morphotypes throughout the Cenozoic.

Furthermore, our results are probably underestimating the real signal since we could not include in our study prominent fossil groups with divergent ecologies like the flightless diving plotopterids or giant flightless auks.

But this is not the only way in which these two major clades contrast!

When we zoomed in the detailed patterns of the skeleton, we more divergences among these major groups!

The hyper-diverse passerines, representing more than half of the total diversity of living species, however:

We have limited evidence that this dichotomy affects other mainly water- and mainly terrestrial clades – calling to a ‘universal’ effect of the environment in avian evolution. Many clades exhibit idiosyncratic patterns revealing the dazzling complexity of avian skeletal forms.

We think that together, all these patterns of evolution reflect how birds interact with their environments and the physical properties of water-linked versus arboreal/terrestrial ecological niches. 🦩🌊 vs🦜🌳🌳

The great array of niches exploited by living waterbirds involve very different locomotory uses of the environment. Transitions among those niches involve complete re-organisations of the musculoskeletal apparatus.

In contrast, landbirds live in more spatially heterogenous environments with plenty of opportunities for finer niche partitioning.

Transitions among niches involve less drastic changes in locomotion and therefore skeletal re-organisations, and affect other aspects of their biology, for instance, divergences in uses of food resources or using different layers of the vegetation cover.

The case of passerines is particularly well-studied as different species diversified by stratifying the use of different canopy layers or the understory.

Our findings also resonate with Simpson’s model of adaptive zones and interzonal versus subzonal evolution.

We suggest that larger discontinuities between waterbird adaptive optima implied that evolution between major adaptive zones (interzonal evolution) was more important for waterbird diversification than it was to landbirds.

For landbirds therefore, evolution within major adaptive zones (subzonal) was more important for their diversification.

This caused changes in subtler aspects of morphology in order to partition niches in an environment where available niches are richer and more ‘continuous’ in the adaptive landscape.

Passerines might be an extreme case of the landbird condition in which even subtle changes in morphology might have allowed them partitioning niches effectively.

But also, they did not partition early their skeletal forms, as the remaining landbirds did, suggesting re-exploration of the same skeletal phenotypes have been important in their evolution. Stay tuned for exciting work on this coming from @LizzySteell.

Our study encourages incorporating the effects of major environments in the macroevolutionary landscape in our expectations from evolutionary models. We are not the first to suggest this, of course, there is, for instance, some evidence of these effects in the body shapes of fish

In our study we scrutinized several aspects of morphology, from shape of individual elements to the form of whole regions and the whole skeleton; and from size proportions of elements to local aspects of variation (e.g., articular facets).

Also, if you are a bit of a bird nerd (like me) you can skim through the SMs where we have extended results for all the detailed patterns of elements throughout the whole skeleton, for every bone and every kind of morphological data.

This research would not have been possible without the funding from the @ERC_Research lead by @BensonLabOxford and my current funding from the @UKRI_News FLF lead by @fieldpalaeo .

Also, Roger’s guidance, teaching and brilliance made up for at least half of this research. Thanks to all the people who contributed to this in one way or another, from segmenting to putting up with me endlessly talking about this and even, for some reason, replying back.

Adiousss

teleost fish paper: academic.oup.com/sysbio/article…