How do palaeontological data refine our understanding of adaptive radiation and the evolution of modern biodiversity?

Swordfishes (needle-nosed predators of the high seas), flounders (gastronomically familiar and bizarrely asymmetrical bottom dwellers), remoras (literal hangers-on that hitch rides on sharks using a suction cup on their heads): few fishes, or indeed vertebrates, show more strikingly different anatomies or modes of life. Divergent as they are, genetic studies indicate that these fishes, as well as several others, are closely related, forming a bough in the tree of life called Carangimorpha. Cases like this, where organisms with shared ancestry branch out over time to assume divergent bodyplans and lifestyles, are known as adaptive radiations. Previous research on this topic has focused on living groups with poor fossil records, like anole lizards, cichlid fishes, and Darwin's famous finches. However, fossils are the only direct means of timing evolutionary events, and yield unique evidence of anatomies pruned from the tree of life by extinction; as such, they are critical in understanding how modern biodiversity came to be. We will study this exceptional group of fishes as a laboratory to not only understand how their specialisations arose, but also explore the ways in which fossils can be especially useful for answering questions of biodiversity and evolution. Specifically, we will ask: (1) what are the steps leading to peculiar carangimorph body 'designs'; (2) when in geological time did these changes occur?; and (3) what do fossils tell us about the speed and manner in which these changes took place?

Fossils are critical in solving these problems. For instance, recent discoveries revealed how flatfishes evolved to have both eyes on one side of their head. Such transitional forms are typically rare, but the diversity of living carangimorphs is complemented by a trove of complete fossils. Modern preparation (chemical treatment or methods akin to sandblasting) and imaging (CT scan) techniques can extract fossils from surrounding rock. We will uncover details of exceptional fossils that show the early stages in the evolution of remarkable adaptations of living carangimorphs, including the rapier-like snout of billfishes and the suction disc of remoras.

Fossils cannot speak for themselves and we cannot simply trace evolution by peeling back rock layers. We must discover the relationships of fossils to living species. We will combine palaeontological data with anatomy and DNA data from modern fishes to place fossils in a tree alongside living relatives, allowing us to reconstruct the transformations leading to specialized modern bodyplans. Including both extinct and living species is also important because fossils influence estimated relationships among living species and vice versa.

To build a timeline for carangimorph evolution, we need to find out when in Earth's history each branch in its family tree split off. Fossilization is a rare event, and so even the oldest fossil of a particular branch might be a relatively late arrival. We therefore need to combine our fossil data with an indirect approach known as the molecular clock. If we know the rate at which genetic mutations build up, we can estimate how long ago living species split from each other and produce a 'time tree': a family tree with an absolute time scale.

With these components in place, we can test how fossils impact our understanding of adaptive radiation and the evolution of biodiversity, using carangimorphs as a test case. Our time tree allows us to apply statistical tools for finding the rate at which anatomical features changed over time. This can be used to see whether change was rapid early in evolutionary history or whether it was slow and gradual, and whether rates varied between marine and freshwater environments. We will conduct our analyses with and without fossils, allowing us to decide whether those based only on modern data might be misleading, and if other biologists should therefore strive to include extinct species in their studies.

Who will benefit?

Our results will interest academic researchers, policy makers, conservation groups, students studying evolution and palaeontology, museums with environment- or biodiversity-related outreach programmes, the media, publishers and the general public.

How will users benefit?

1. THE ACADEMIC COMMUNITY
See 'Academic Beneficiaries'.

2. POLICY MAKERS AND CONSERVATION GROUPS
By establishing a 'deep time' perspective on a group that includes many living species threatened by overfishing, our research illustrates the evolutionary time scales required to generate modern biodiversity, and provides additional motivation for conservation efforts. Additionally, our refined picture of relationships among these fishes will represent a key resource for conservation biologists implementing strategies intended to maximize the preservation of phylogenetic diversity.

3. STUDENTS
Undergraduates will benefit directly from our research programme. We will also integrate the results of this project into taught courses at Oxford and Yale as well as UCL, Imperial, Cambridge, Leiden, where team members have given guest undergraduate lectures. We will develop small, self-contained 'spin-off' projects that can be advertised to Oxford undergraduates in Earth Sciences (MEarthSci) and Zoology (Final Honours School Project), and students completing M.Res work at NHM. Such projects could focus on individual specimens and CT datasets, with results prepared for publication with the PI, and Co-I, PDRA, and project partners.

4. MUSEUMS
The Oxford University Museum (OUM), and The Natural History Museum (NHM) have outreach and education programs that draw on cutting edge results from associated academics. The PI and Co-Is have collaborative relationships with these museums and will use the results of the project as in talks, exhibitions, and other events such as 'Nature Live' (NHM), 'Friends of the NHM' (NHM), and 'Science Saturdays' (OUM). Museums will also benefit from entry of specimen data into digital databases (NHM KEEmu) and preparation work that adds scientific value to fossils.

5. MEDIA AND PUBLISHERS
We have a strong record of interaction with the media, with coverage of research in the international press, radio, and television (see PI Friedman CV). Our work will provide new ideas and results that will feed into these media and publishing activities. We will engage with these users through conventional press releases, plus announcements made via the Oxford Science Blog (http://www.ox.ac.uk/media/science_blog/), which regularly features research output from PI Friedman.

6. GENERAL PUBLIC
Our work will benefit the public in terms of UK culture and quality of life. Our target clade of anatomically bizarre but generally familiar fishes provides an excellent opportunity to engage with the general public (including school children) on topics such as global change, evolution, conservation and biodiversity. Second, our focus on exceptional British fossils from the London Clay will highlight the significance of this aspect of the UK's natural heritage. We will engage with the public from the beginning of work via press releases, talks, and outreach through NHM and OUM (see above), as well as contributed columns to the Zoologists' Club newsletter for the University Museum of Zoology, Cambridge.

7. STAFF ON THE PROJECT
The PDRA will develop a number of transferable skills that can be broadly applied. These include: writing and oral presentation; programming and statistical analysis; molecular and morphological systematics; science communication; advanced imaging techniques.