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Unravelling the scenario of early vertebrate evolution through computational analysis of the fossil record

Periodic Reporting for period 1 - EarlyVertEvo (Unravelling the scenario of early vertebrate evolution through computational analysis of the fossil record)

Okres sprawozdawczy: 2019-06-01 do 2021-05-31

Debate over the origin of vertebrate bodyplan has occupied biologists and palaeontologists alike for centuries but discussions around this topic have been hindered because living vertebrates are unrepresentative of the ancestral lineages in which the bodyplan was established. Major transitions in early vertebrate evolution have been correlated with a long-term ecological trend from suspension feeding towards increasingly active lifestyles. However, most previous morpho-functional interpretations largely rely on speculation and these ecological explanations of evolutionary events have generally been regarded as untestable as theories. The recent emergence of new virtual techniques in palaeobiology provides for the first time the opportunity to perform rigorous computational and physical examination to test these hypotheses.

In this context, the overall aim of my research programme was the joint application of an array of state-of-the-art techniques in palaeobiology to fossil stem-gnathostomes in order to elucidate the ecological scenarios in which the major groups of vertebrates emerged and to shed light onto the underlying selective forces that drove the main evolutionary transitions of the group. The specific objectives of the project can be summarized as:

- Summarizing and numerically describing the morphological diversity of early vertebrates within a phylogenetic and temporal framework on which to base evolutionary hypotheses regarding morphological disparity or functional and macroecological aspects.
- Obtaining a comprehensive and representative collection of realistic 3D virtual models of early vertebrates on which to empirically test these hypotheses by means of computational techniques.
- Assessing ecological and hydrodynamic aspects in early vertebrates by means of the novel application of CFD on this group.
- Contextualizing these results within a macroevolutionary scenario in order to ascertain if the evolution of vertebrates was characterised by a trend towards increasingly active lifestyles (according to classical hypotheses) or if more complex evolutionary patterns took place.
(1) In a first step, we have assessed the congruence between two non-mutually exclusive approaches to characterize morphological variation (disparity) in the fossil record: (1) quantitatively, through geometric morphometrics; and (2) in terms of discrete, ‘cladistic’, or categorical characters (Ferrón et al. 2020, Palaeontology, 63(5)).
(2) Using these approaches, we have characterized the morphological diversity of all major stem-gnathostome clades (Ferrón et al. 2020, Palaeontology, 63(5); Ferrón et al. 2020, Curr. Biol., 30(23); Ferrón et al. 2021, Proc. Royal Soc. B, 288(1943)).
(3) We have generated a collection of more than 100 three-dimensional virtual models with representatives of all major stem-gnathostome clades.
From the above framework and database, we have performed functional tests by means of computational fluid dynamics elucidating some fundamental aspects to understand early vertebrate evolution:
(4) The headshield morphology in several groups of ostracoderms (stem-gnathostomes) is compatible with a diversity of hydrodynamic efficiencies including passive control of water flow around the body which could have increased versatility for adopting diverse locomotor strategies (Ferrón et al. 2020, Curr. Biol., 30(23)).
(5) We revealed similar hydrodynamic performance among morphologically convergent species (Ferrón et al. 2021, Proc. Royal Soc. B, 288(1943)).
(6) We have found that a number of the characters typically used to infer the evolutionary relationships among galeaspids, osteostracans and jawed vertebrates are convergent in nature, potentially obscuring understanding of the assembly of the gnathostome bodyplan (Ferrón et al. 2021, Proc. Royal Soc. B, 288(1943)).
(7) We have revealed that the jawless relatives of the earliest jawed vertebrates reached the limits of their potential ecological diversity—overcome by jawed vertebrates and their later innovations (Ferrón et al. 2021, Proc. Royal Soc. B, 288(1943)).
(8) In parallel, we have provided a refined view of the ecological context in which vertebrate and gnathostome body plans were assembled (Ferrón and Donoghue, Science Advances in rev.).

The researcher has produced several scientific publications, including a number of published papers as well as other at various stages between acceptance and final stages of preparation:

Ferron et al. (2020). Palaeontology, 63.
Ferrón et al. (2021). Proceedings of the Royal Society B, 288.
Ferrón et al. (2020). Current Biology, 30.
Ferrón, H. G., & Donoghue, P. C. (in rev.). Science Advances.
Ferrón, H. G. (2019). Journal of Vertebrate Paleontology, 39.
Cooper et al. (2020). Scientific reports, 10.
Ballell, A., & Ferrón, H. G. (2021). Scientific reports, 11.
Herraiz et al. (2020). Biology Letters, 16.


Further, the researcher has attended several international congresses to disseminate the results and has also participated in several outreach activities including online events and different radio podcast.
Integration and analysis of these data have produced the first comprehensive test on the ecological scenario that underlid early vertebrate evolution and the assembly of gnathostome body plan based on computational techniques. We have contributed importantly to elucidate two long-lasting hypotheses on the nature of early vertebrate evolution. First, we have addressed the hypothesis that early (jawless) vertebrates were ecologically constrained until released by the key innovation of jaws which precipitated the ecological diversification of the group. Through analyses of morphological disparity, virtual modelling and Computed Fluid Dynamics, we show that even though jawless stem-gnathostomes lacked jaws and key locomotor innovations such as pelvic fins and a mineralised vertebral skeleton, they were already adapted to diverse ecologies through morphological adaptations for passively controlling flow around the body, conferring greater manoeuvrability and versatility than previously thought. Secondly, we have assessed the “New Head Hypothesis” which proposes that the assembly of vertebrate and gnathostome body plan was underpinned by a long-term trend towards increasingly active food acquisition and enhanced locomotory capabilities culminating with the emergence of jawed lineages. Through implementing phylogenetically-informed models for predicting swimming speeds from caudal fin morphology, ancestral character state reconstruction and evolutionary model-fitting, we show that the evolution of locomotory capabilities in early vertebrates followed complex trajectories, with no support for a trend towards more active lifestyles in the line leading to jawed groups.
Reconstruction of different stem-gnathostomes showing their ecologies.