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Behaviour-Connect: Testing hypotheses on the behavioural drivers of connectivity in the marine environment through novel Bayesian models

Periodic Reporting for period 1 - Behaviour-Connect (Behaviour-Connect: Testing hypotheses on the behavioural drivers of connectivity in the marine environment through novel Bayesian models)

Reporting period: 2016-03-16 to 2018-03-15

Connectivity is broadly defined as the exchange of individuals between populations. Assessment of connectivity is a key goal in ecology, evolution, and conservation biology. At the ecological level, connectivity is key in the persistence and resilience of populations. At the evolutionary level, connectivity influences local adaptation.
In the marine environment, ecologists have primarily focused on biophysical models of larval exchange when investigating connectivity, because of the importance of this process on exploited or commercial species. This has diverted attention from the potentially important role of behaviour as a driver of connectivity in the marine environment. Aspects of a species behaviour, such as migratory fidelity, social structure and feeding specialisations, can play a strong role in shaping connectivity and gene flow that has been largely ignored in connectivity studies to date.
This knowledge gap has been sought to be addressed by simultaneously harnessing leading empirical methods, micro-chemical markers and genomics, and integrating these into a novel Bayesian framework for testing hypotheses about the behavioural drivers of connectivity. The novel model system for this work, southern right whales (SRWs), shows maternally transmitted preferences for migratory destinations that could influence connectivity. The combination of well-described life history traits and lack of barriers to dispersal makes the SRW an ideal species in which to investigate the importance of behaviour on connectivity. A global collaboration on the species, exemplified by a recent publication (Carroll et al 2018, Heredity), has been developed to study the role of behaviour in population structure and connectivity in the species, and led to the formation of global SRW genomic and stable isotope database. The novel Bayesian model has been developed and presented at an international conference in 2017. Work is currently ongoing to integrate the genomic and stable isotope data with the new model. The impact of this work is shown by the invitation of Dr Carroll to the UNEP/CMS Workshop on Conservation Implications of Animal Culture and Social Complexity, and the use of the SRW as an exemplar at this workshop for migratory culture.
LABORATORY WORK AND ANALYSIS
I have developed an international network involving over 25 researchers from 10 countries studying southern right whales (SRWs) that represent the species' 5 major extant wintering grounds. High-resolution genomic markers (single nucleotide polymorphisms (SNPs)) have been generated for over 400 samples, using restriction associated digest (RAD) tag sequencing. Stable carbon and nitrogen ratios were also generated for samples, as indicators of foraging ecology in SRWs.
These data were used to investigate the influence of complex behaviours on connectivity, as it can impact the current methods and limit our understanding on this critical metric in the marine species. Working with Prof. Gaggiotti, a novel Bayesian model has been developed to model culturally inherited migratory behaviour in a population assignment framework. This model was presented at the Evolution conference in 2017 and work is ongoing to rigorously test the model and integrate the genomic and stable isotope data.

DISSEMINATION AND COMMUNICATION OF RESULTS
Oral conference presentations:
(1) Carroll, E. L. & O. Gaggiotti. 2017. Testing how migratory fidelity influences connectivity. Evolution, USA, 2017
(2) Carroll, E. L. 2017. Genetic and genomic monitoring with minimally invasively collected samples. Next Gen Bioinformatic User Group, Scotland, 2017
(3) Carroll, E. L. M. Olsen, C. Morris, et al. 2017. Harbour seal genelemetry: Understanding source-sink dynamics across the United Kingdom by combining population survey, genetic and telemetry data. European Cetacean Society Conference, Denmark, 2017
(4) Carroll, E. L., R. Alderman, J. Bannister, et al, 2016. Hierarchical circumpolar population structure and reduced connectivity between ocean basins in the SRW. IMarCO Conference, Scotland, 2016

Invited workshop participation/presentation:
(1) TTGAC workshop on Population Variation Genetics workshop, UK, May 2016.
(2) NIMBIOS Investigative Workshop Next Generation Genetic Monitoring, USA, November 2016
(3) UNEP CMS Workshop on Conservation Implications of Animal Culture and Social Complexity, Italy, April 2018
(4) Scientific Committee meeting of the International Whaling Commission, Slovenia, April 2018

Public engagement:
Press release coincident with publication of Carroll et al 2018, Heredity.
Contributor to the Royal Society of Edinburgh’s Young Academy of Scotland Research the Headlines blog (https://researchtheheadlines.org)
Carroll, E. L., 2017. Molecular Ecology in Marine Mammals. Public lecture, Spain, May 2017
Carroll, E. L., 2017. How does migratory culture influence connectivity in Australian right whales? Insight from genetic and stable isotope data. Australian Marine Mammal Centre workshop on southern right whales, Australia, Mar. 2017
1. Further advance the state of the art in population and conservation genomics:
The recognition of this work as further advancing the state of the art in population and genomics is highlighted by the invitations I have received to present and participate in genomic and molecular ecology related workshops, and the invited review papers I have contributed to and led.

2. Recognition of the role of non-human culture in animal conservation:
The work conducted into SRWs as part of this research project is being used to highlight the importance of the role of culture in conservation. SRWs show migratory culture, whereby offspring learn their mothers preferred migratory destinations during a period of prolonged natal care. My work has shown that this has influenced genetic population structure of southern right whales across its migratory network, and that it is shaping recovery and recolonisation of the species after whaling. The work conducted as part of the Marie Curie goes beyond descriptions and correlations and provides a framework for explicitly testing for the impact of migratory culture in population assignment and connectivity. The importance of the southern right whale as a model organism for migratory culture is shown by invitation to participate and present to the United Nations Environmental Program CMS Workshop on Conservation Implications of Animal Culture and Social Complexity, which could shape global policy.

3. Explicitly integrating culture into models of population assignment and connectivity:
Behaviour can strongly impact local patterns of extinction and recolonisation, thereby affecting large-scale population dynamics and connectivity. The integration of life history traits into models of gene flow and population structure has been noted as an important avenue for future investigation. This will represent the first time genetic and isotopic data will be evaluated in an integrated framework with an explicit behavioural model so as to assess connectivity. Indeed, it is only possible to test hypotheses on the behavioural drivers of connectivity in this model system by combining data types, creating a strong aspect of originality and innovation. This model is currently undergoing rigorous testing using simulated data and will then integrate the global genomic and stable isotope datasets.
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