Does developmental plasticity direct the divergence among species?

Selection pressure is determined by ecological opportunity, but the response to selection depends on individual form (1). Individual form matters because individuals in species are characterised by a distinctive set of codependent traits. Selection on one trait can therefore generate a response to selection in others. This evolutionary constraint due to trait covariation is imposed by heredity or natural selection and can limit adaptation by channelling evolution in the direction of least evolutionary resistance (2) characterised by abundant phenotypic variability (3). Allometric relationships of size-shape covariance are classic lines of least evolutionary resistance. Allometries have been categorised into within-individual, among-individual and among-species scales (reviewed by 4), making them an ideal framework to investigate how variation among individuals generates variation among species.
Contradicting recent re-analyses of over 300 animal taxa (5,6), Brombacher, Ezard et al. (invited resubmission, American Naturalist) found a decoupling between among-individual and among-species allometries in 12,633 individuals of two- species of planktonic foraminifera exposed to the intensification of Northern Hemisphere glaciation during the Pliocene. Neither published study (5,6) sampled through a major climate transition. The generality of when among-individual and among-species allometries become decoupled, as well as the macroevolutionary consequences of this decoupling are testable with PISTON's data from WP2, WP4 and WP5 for the first time.
Our overarching hypothesis for PhD1 is that within-individual changes catalyse the breakdown in among-individual and among-species allometries. This question is one of the oldest in evolutionary biology: von Baer's third law states that individuals in different species become increasingly dissimilar from one each other during development, implying we should see changes at the within-individual level before species diverge. In reality, variation among individuals is a dynamic force that represents the ghost of evolution past. Under supervision of Watson and Ezard, PhD1 will extend well-developed learning theory models, familiar in computer science, to formally characterise how the cumulative outcome of historical selection facilitates future adaptability (7). Watson's existing theoretical models find that developmental correlations will align with directional selection creating 'lines of least resistance' (2) that facilitate directional adaptive change (7,8). This PhD project will extend learning theory with adaptive dynamics models (9) parameterised by foraminiferal trait distributions and environmental reconstructions to address three overarching questions:
1: Does within-species plasticity precede and direct divergence among species along lines of least evolutionary resistance? 2: Are certain parts of the life-course (e.g., a developmental window early in life prior to canalisation) more predictive of divergence among species than others?
3: How do historical environmental change and intraspecific variation interact to determine whether the allometric relationships will break down across individual, population and species scales?
References: (1) Lande & Arnold 1983 Evolution 37, 1210. (2) Schluter 1996 J. Evol. Biol. 50, 1766. (3) Hunt 2007 Evolution 61, 1560. (4) Pelabon et al. 2014 Ann. New York Acad. Sci. 1320, 58. (5) Voje et al. 2014 Evolution 68, 866. (6) Firmat et al. 2014 Phil. Trans. R. Soc. B 369, 20140057. (7) Watson & Szathmary 2016 Trends Ecol. Evol. 31, 147. (8) Watson et al. 2014 Evolution 68, 1124. (9) Doebeli & Dieckmann (2000). Amer. Nat. 156, S77.

PISTON takes an unprecedented transdisciplinary approach to investigate how new species form. Species are the foundation of biodiversity. The House of Lords Systematics & Taxonomy review identified biodiversity's critical underpinning of an extensive array of natural environment research ranging from blue skies evolutionary questions, particularly into charismatic "missing links" that reveal how differences among individuals generate differences among species, to applied questions such as ecosystem service provision (i.e., the benefits we derive from natural ecosystems) and global health threat mitigation.

PISTON has been designed as a set of interrelated work packages that will integrate to more than the sum of their individual parts to impact policy, public health, industry and the general public. PISTON investigators are active in all these sectors and will build on and further develop existing relationships and activities.

Members of PISTON have a strong track record of contributing to Intergovernmental Panel on Climate Change (IPCC) reports. Our unprecedented data, focusing on the pivotal link between organism and environment and from the last interval when the world was 2-3 degrees warmer than it is today, can contribute to future IPCC reports in this area. Foster (Contributing Author) and Schmidt (Chapter Lead Author; Co-author of Summary for Policymakers) will co-ordinate impact in this area.

Proprietary versions of WP1 computer vision algorithms have successfully delineated the ball and socket of hip joints as a diagnostic to improve hip replacement therapy, which indicates their potential for wider healthcare benefits for the general public. The PISTON team has considerable experience working with industry (Sinclair with Nikon to develop bespoke biological and medical tools) and the public sector (Nixon on, e.g., automated gait recognition) and will draw on this experience to ensure the open-source PISTON outputs are carefully described, annotated and made accessible in toolbox form to the broadest possible community of end-users.

Taxonomic revisions through refined dating and age control will directly impact foraminiferal specialists in commercial operations, particularly the oil industry. The statistical approaches we propose minimise subjective choices, which adds repeatability and transparency across end-users. We will build on existing networks: Wade (NE/N017900) and Wilson (PI: NE/K007211 and NE/K014137) name PetroStrat, Network Stratigraphic, Shell, RPS Energy and Neftex-Halliburton as Industrial Partners on current awards. Wade will act as Industry Impact Champion (1.5% costed time) to incorporate PISTON data and curate the Mikrotax illustrated online portal. In addition to working with External Advisory Board member Haydon Bailey (Network Stratigraphic) to deliver Industrial impact, we will invite further industrial partners to the second scientific scoping workshop in Year 3 (£2500 budgeted for one UK and one international).

All Research Staff will participate in Public Engagement activities during PISTON in areas of particular appeal to each individual. In particular, we will work with Ellen Dowell, a Science Communicator, interdisciplinary facilitator and current collaborator of PI Ezard (NE/J018163), to run interactive workshops in Einstein's Garden at the Green Man Festival in Year 3 (led by Aze), which we will then run subsequently at exhibitions through applications to the NERC Science Festival, Royal Society Summer School and local science festivals in our regions. These hands-on workshops will let festival-goers see evolution in action and contribute to an animated "flick book" style-film based on the divergence into new species (£3000 budgeted). This film will ensure legacy and impact beyond the festival fence.