ECOLOGICAL OPPORTUNITIES AND SPECIALIZATIONS SHAPED GENETIC DIVERGENCE IN A HIGHLY MOBILE MARINE TOP PREDATOR

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Studying cetacean population structure: interest and challenges

Cetaceans are highly mobile mammals which can show various levels of genetic and ecological structures as well as morphological variations both at large and very fine scales (e.g. Sellas et al. 2005; Fontaine et al. 2007; Viaud-Martinez et al. 2008; Foote et al. 2009; Ansmann et al. 2012b; Wilson et al. 2012; de Bruyn et al. 2013). They can have complex social structures that vary from solitary individuals in mysticetes, where only mothers and calves form stable bonds (e.g. Valsecchi et al. 2002) to stable matriarchal societies for pilot whales and killer whales (Amos et al. 1993; Pilot et al. 2010). They are therefore particularly suitable models to study social, ecological and genetic structures and their interaction in shaping structuration patterns.
Nevertheless, as they spend most of their time underwater, studying cetacean structuring patterns is particularly challenging. Individual monitoring using the marks on the fins through photo-identification that is described in more details in Chapter 2 enables the study of social structure and demography (Figure 1.1). However, field work is strongly constrained by sea conditions. In addition, while photo-identification monitoring is well suited for coastal areas and relatively small populations, its utility in offshore waters where small cetacean populations are generally large and highly mobile and their distribution largely unknown, is limited.

Taxonomy and variations in ecology, morphology and genetic structure

The taxonomic status of bottlenose dolphins (Tursiops sp.) remains unresolved and the genus is not monophyletic (the taxonomy of Delphininae was recently reviewed in Perrin et al. 2013). Two species are recognized: common bottlenose dolphins Tursiops truncatus (Montagu 1821) and Indo-Pacific bottlenose dolphins Tursiops aduncus (Ehrenberg 1832, LeDuc et al. 1999; Wang et al. 1999, 2000b, a). While common bottlenose dolphins have a worldwide distribution range (Figure 1.3), Indo-Pacific bottlenose dolphins are only found in warm temperate to tropical Indo-Pacific areas. A third species has been described in South-East Australia (the Burrunan dolphin, T. australis, Charlton-Robb et al. 2011) but its validity is debated. A subspecies of common bottlenose dolphin is recognized in the Black Sea, T. Truncatus ponticus (Viaud-Martinez et al. 2008). Here, we will focus on common bottlenose dolphins, although there are references to both common and Indo-Pacific bottlenose dolphins.
Common bottlenose dolphin feeding ecology and morphology is variable across its distribution range. Two distinct ecotypes, i.e. “coastal” and “pelagic” have been described in the North-West Atlantic (NWA) and in the North-East Pacific (NEP, reviewed in Curry & Smith 1998). We define “pelagic” here as dolphins mainly occurring in deep waters (i.e. deeper than 200 m). The term “pelagic” is interchangeably used with “offshore” in the literature. We choose “pelagic” to refer to individuals occurring in deep-waters, even if they are close to shore (e.g. the Strait of Gibraltar, Spain). We acknowledge that pelagic can also mean “live in the water mass” in contrast to benthic. “Coastal” refers to individuals mainly sighted in shallow waters (less than 200 m, but in majority less than 40 m deep).
In the NWA and the NEP, pelagic and coastal bottlenose dolphins are genetically, ecologically and morphologically distinct and show different parasite loads (Walker 1981; Duffield et al. 1983; Hersh & Duffield 1990; Mead & Potter 1995; Curry & Smith 1998; Hoelzel et al. 1998b; Walker et al. 1999; Segura et al. 2006; Kingston et al. 2009; Barros et al. 2010; Perrin et al. 2011). While genetic differentiation is found in both areas, pelagic and coastal ecotypes are monophyletic for mitochondrial DNA only in the NWA (Curry & Smith 1998; Hoelzel et al. 1998b; Segura et al. 2006; Kingston et al. 2009). In the North-East Atlantic (NEA), although ecotype differentiation has been suggested, it was not tested explicitly (e.g. Fernandez et al. 2011a; Mirimin et al. 2011).
Fine-scale genetic structure is observed in coastal and inshore waters worldwide, presumably as a result of philopatry and habitat/resource specializations (e.g. Sellas et al. 2005; Mirimin et al. 2011). Although often resident in inshore and coastal areas, large-scale movements have been reported, both in coastal and pelagic waters (Defran et al. 1999; Wells et al. 1999; Robinson et al. 2012).

Life-histories and social structure

Bottlenose dolphins can live up to at least 57 years for females and 48 years for males. They reach sexual maturity between 5 to 13 years for females and between 8 and 14 years for males. Calves usually stay from 3 to 5 years with their mother, with separation often coinciding with the birth of the next calf. Gestation period lasts 12 months and inter-birth intervals usually range from 3 to 6 years (reviewed in Wells & Scott 1999; Connor et al. 2000). Information on the life-history mainly originates from the well-studied population of Sarasota Bay (coastal ecotype of the NWA) but might vary slightly across the geographical range of the species. Nevertheless, bottlenose dolphins are long-lived animals with a low reproductive rate.
Bottlenose dolphin (Tursiops sp.) social structure is defined as fission-fusion, where group composition changes on an hourly or a daily basis. Besides having a majority of short-term associates, individuals can also share some strong and long-term relationships (Connor et al. 2000). Group sizes, patterns of relationships within and between sexes, relatedness, and temporal stability of associations can be variable across the wide geographical range of the species (e.g. Connor et al. 2000; Krützen et al. 2003; Lusseau 2003; Wiszniewski et al. 2010b; Augusto et al. 2011; Connor et al. 2011; Wiszniewski et al. 2012a). The most detailed information came from the long-term studies of populations of Australia (Shark Bay, Connor et al. 2000) and Florida (Sarasota Bay, Wells et al. 1987). Social structure variations will be discussed in more details in Chapters 3 and 4.

Bottlenose dolphins in the North-East Atlantic, distribution and conservation status

In the North-East Atlantic, bottlenose dolphins are observed in both coastal and pelagic waters. They can form resident communities of tens to a few hundreds of individuals in bays, estuaries or coastal areas (Figure 1.4., e.g. Liret 2001; López 2003; Pesante et al. 2008; Augusto et al. 2011; Berrow et al. 2012; Cheney et al. 2012). Mobile coastal communities have been recorded around Ireland and in the Gulf of Cadiz (O’Brien et al. 2009; Giménez et al. 2013). Resident individuals are observed in deep waters of the Strait of Figure 1.4. Mobile and resident bottlenose dolphin communities inferred using photo-identification data in the North-East Atlantic and the Mediterranean Sea. The list may not be exhaustive. The Normano-Breton gulf (English Channel) population is highlighted in red.
Bottlenose dolphins also occur in pelagic waters in particular along the shelf edge where abundance estimations are tens of thousands of individuals (Figures 1.5a and 1.5b, Certain et al. 2008; Hammond et al. 2009; Hammond et al. 2013).

Molecular markers: mitochondrial DNA and microsatellites

Mitochondrial DNA is a small circular molecule which is present in numerous copies in animal cells. It is haploid and mostly maternally inherited although heteroplasmic individuals (i.e. for which mitochondrial DNA was biparentally inherited) can be observed in different proportions in some taxa (e.g. Zouros et al. 1994; Vollmer et al. 2011). As it is haploid, there is generally no recombination (but see Eyre-Walker 2000; Ujvari et al. 2007). Evolution rate is five to ten times faster than nuclear DNA in mammals (Moritz et al. 1987), with an average mutation rate of 1 x 10-8 per site per year, making it useful in population genetics and phylogenetic studies. Mitochondrial DNA is composed by different regions which have different evolution rates including the control region which is the most variable and rapidly evolving part and thus of interest for population genetic studies. Estimates of mutation rates for the control region of cetaceans vary from 0.5 x 10-8 to 1.3 x 10-6 per site per year (Hoelzel et al. 1991; Harlin et al. 2003; Alter & Palumbi 2009; Fontaine et al. 2010).
As it is haploid and maternally inherited, effective population size at mitochondrial loci is four times lower than at nuclear loci. Mitochondrial genome is therefore more sensitive to genetic drift and integrates demographic events like population expansions or bottlenecks* since a longer time than nuclear markers.
Polymorphism in the sequence is detected through sequencing. Each haplotype is a unique sequence. Different haplotypes differ by one or more nucleotides because of substitutions, deletions or insertions.

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Non-bayesian clustering methods

Both TESS and STRUCTURE rely on genetic model assumptions (e.g. Hardy- Weinberg and Linkage Equilibria) and are therefore based on an “idealized” population model. With large datasets, they may require long computational times, due to the nature of MCMC simulations, in particular for STRUCTURE. For example, the MCMC may need tens of thousands of steps to reach convergence. In addition, an initial portion of the MCMC should be discarded to avoid the influence of initial values on the posterior distributions. DAPC (Discriminant Analysis of Principal Components) is an alternative method that does not rely on any genetic model assumptions (Jombart et al. 2010). It tries to cluster individuals based on genetic similarity, with genotypes being treated like a classical multivariate dataset. In DAPC, the number of clusters is first determined using a K-means method that aims at determining populations of individuals by minimizing within-population genetic variation. As in the Bayesian clustering methods, the K-means algorithm is ran with different numbers of putative populations. BIC (Bayesian Information Criterion) is used to determine the most likely number of populations. Then, the data are transformed using a Principal Component Analysis which summarizes the overall variability among individuals both among and within populations. This step ensures that the numbers of variables (i.e. alleles) are lower than the number of individuals and that the variables are not correlated. The Discriminant Analysis is applied on the Principal Components; it aims at partitioning genetic variation so that among-population variation is maximized while within-population variation is minimized. Individuals are assigned probabilistically to each population. DAPC has the advantage to have a fast computational time, even for large datasets. In addition, it has been shown to be as efficient as STRUCTURE (Jombart et al. 2010). DAPC also provides a visual representation of the structure between the populations, i.e. the scatterplots, which helps to understand the patterns of genetic structure (see Figure 2.6, Jombart et al. 2010).

Coalescent theory and population demographic history analyses

Coalescent theory is the base of numerous methods or models that aim at reconstructing the past history of populations such as their size, growth rate, gene flow or their patterns and times of divergence using molecular markers. Here, I will explain the general theory and the specific method that was used in this dissertation to reconstruct the demographic history of bottlenose dolphins in the North-East Atlantic in Chapter 6.
Classical population genetics is a prospective approach which aims at predicting the future of allele frequencies in populations. In contrast, coalescent theory is a retrospective approach which aims at reconstructing the genealogy of a sample of genes going backwards in time to the Most Recent Common Ancestor (MRCA, Figures 2.7a to 2.7c, reviewed in Nordborg 2001). It should be noted that in a coalescent framework, we work with genes, not individuals. In any population, the probability for two genes to coalesce follows an exponential probability distribution. As we get backwards in time, the number of genes will decrease and the time to the next coalescent event (represented by the branch length) will increase. As most mutations can be considered neutral, they can be added afterwards following a Poisson distribution with parameter the length of branches.

Table of contents :

CHAPTER 1 GENERAL INTRODUCTION
1) Interaction between social, ecological and genetic structures
2) Drivers of structure
a) Social structure
b) Ecological structure
c) Genetic structure
3) Conservation implications
4) Study model: bottlenose dolphin and research questions
a) Studying cetacean population structure: interest and challenges
b) Why studying bottlenose dolphins?
c) Taxonomy and variations in ecology, morphology and genetic structure
d) Life-histories and social structure
e) Bottlenose dolphins in the North-East Atlantic, distribution and conservation status .
f) Research questions
g) Manuscript organization
CHAPTER 2 METHODOLOGICAL BACKGROUND
1) A combination of approaches: from recent to evolutionary time scales
a) Photo-identification
b) Ecological and diet indicators
c) Morphometrics
d) Molecular markers: mitochondrial DNA and microsatellites
2) Statistical analyses of molecular markers
a) Bayesian statistics
b) Genetic structure
c) Coalescent theory and population demographic history analyses
CHAPTER 3 SOCIAL STRUCTURE AND ABUNDANCE OF COASTAL BOTTLENOSE DOLPHINS IN THE NORMANO-BRETON GULF, ENGLISH CHANNEL
1) Introduction
2) Material and methods
a) Surveys and photo-identification
b) Social structure
c) Abundance
3) Results
a) Survey effort and photo-identification
b) Social structure
c) Community size
4) Discussion
a) A fission-fusion social structure
b) Possible ecological drivers of large group sizes
c) Division in three social clusters
d) Abundance
e) Monitoring and conservation
CHAPTER 4 EVALUATING THE INFLUENCE OF ECOLOGY, KINSHIP AND PHYLOGEOGRAPHY ON THE SOCIAL STRUCTURE OF RESIDENT COASTAL BOTTLENOSE DOLPHINS
1) Introduction
2) Material and methods
a) Boat surveys, biopsy sampling and photo-identification
b) Social structure
c) Genetic analyses
d) Genetic population structure
e) Ecological population structure
f) Influence of relatedness, sex and ecology on association patterns
3) Results
a) Biopsy sampling
b) Genetic population structure
c) Ecological population structure
d) Influence of relatedness, sex and ecology on association patterns
4) Discussion
a) Three social and ecological clusters but a single population
b) Ecology but not kinship influences social structure
c) Influence of phylogeography on social structure
d) Drivers of social structure and interest of combining approaches
CHAPTER 5 HABITAT-DRIVEN POPULATION STRUCTURE OF BOTTLENOSE DOLPHINS IN THE NORTH-EAST ATLANTIC
1) Introduction
2) Material and methods
a) Sample collection, DNA extraction and sexing
b) Microsatellite genotyping and validity
c) Mitochondrial DNA sequencing
d) Population structure
e) Nuclear genetic differentiation and diversity
f) Mitochondrial DNA differentiation and diversity
g) Recent migration rates
h) Effective population sizes
3) Results
a) Microsatellite validity
b) Drift prediction model
c) Population structure
d) Genetic differentiation and genetic diversity in the NEA
e) Recent migration rates
f) Effective population sizes
4) Discussion
a) Hierarchical structure
b) Possible drivers of population structure
c) Effective population size estimates: small coastal vs large pelagic populations.
d) Management implications
e) Ecotype delineation and future directions
CHAPTER 6 ECOLOGICAL OPPORTUNITIES AND SPECIALIZATIONS SHAPED GENETIC DIVERGENCE IN A HIGHLY MOBILE MARINE TOP PREDATOR
1) Introduction
2) Material and methods
a) Genetic inference of the population demographic history
b) Ecological and morphological characterization of ecotypes
3) Results
a) Genetic inference of the population demographic history
b) Morphometric analyses
c) Stable isotope analyses
d) Stomach content analyses
4) Discussion
a) Ecologically-driven demographic history of bottlenose dolphins in the North-East Atlantic
b) Niche specializations maintain genetic divergence between coastal and pelagic ecotypes
c) Absence of strong influence of ecology on external morphological traits
d) Possible differential stage of speciation in the North Atlantic
CHAPTER 7 GENERAL DISCUSSION
1) Synthesis of the results
a) Bottlenose dolphin social, ecological and genetic structures in the Normano-Breton gulf
b) Bottlenose dolphin population structure in the North-East Atlantic
2) Structuring patterns of bottlenose dolphins and other mobile social predators: interaction between ecology, sociality and genetics
a) The central role of ecology in shaping the structure of populations
b) Social behavior likely strengthens the influence of ecology on genetic structure
c) Influence of evolutionary history on social structure
3) Combination of scales and approaches to study the structure and evolution of populations
a) Combination of spatial scales
b) Combination of approaches
4) Implications for conservation
a) Conservation of bottlenose dolphins in the Normano-Breton gulf
b) Conservation of bottlenose dolphins in the North-East Atlantic
c) Management implications beyond bottlenose dolphins
5) Perspectives
REFERENCES ..

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