behaviourAL VARIATIONS, ADAPTATION & EVOLUTION

Response to rapid environmental change

Organisms have been adapting to novel and changing environments for millennia, long before the arrival of humans. Differences in how species survive in the face of glacial advances, changing atmospheric composition, faunal interchanges and catastrophic events such as meteor impacts have shaped the composition of modern communities and ecosystems (Snell-Rood 2013). But the key difference between adaptation over the evolutionary history of Earth and adaptation in recent history is the pace of change organisms have had to keep up with. Today, organisms are presented with novel and rapidly changing environments with the spread of invasive species, climate change, pollutants, habitat loss or fragmentation, conversion to agriculture and urban areas, increased human harvesting, exposure to novel biotic (e.g., predators, competitors, pathogens) or abiotic (e.g., pollutants) stressors and/or availability of novel, inappropriate resources. Such human-induced rapid environmental changes pose a serious threat to the persistence of many species and populations.

A major question is therefore to understand how populations and species respond to such human-induced rapid environmental change (Sih et al. 2011; Tuomainen & Candolin 2011). Why some organisms can successfully cope with human-induced rapid environmental change whereas most cannot remains obscure. This information will be crucial to evaluate species probability of persistence at both short and long-term.

To cope with environmental change, organisms have basically 3 options:

• niche tracking (distribution range shift), which involves avoiding the new environment and tracking suitable conditions;

• phenotypic plasticity, which is defined as the ability of a single genotype to express varying phenotypes (phenology, morphology, physiology, or behavior) when exposed to different environmental conditions;

• adaptive evolution (microevolution), which involves changes in allele frequencies at loci that result in increased fitness in the new environment.

A change in phenotype over time as environmental conditions change could be the result of either evolution or plasticity (Franks et al. (2014). Plasticity and adaptive evolution are not mutually exclusive (Nicotra et al. 2010). Global change may induce the evolution of plasticity, with traits evolving to become more or less plastic as environmental conditions change (Springate et al. 2011). Both plastic and evolutionary responses to environmental change can influence population persistence, and both may or may not be adaptive (Ghalambor et al. 2007). Plasticity and adaptive evolution may interact. Plasticity can hinder evolution by dampening the effects of selection, or promote evolution by allowing population persistence under changing conditions (Chevin & Lande 2010, 2011; Chevin et al. 2010, 2013; Crispo et al. 2010).

NICHE TRACKING

But niche tracking is not always possible. Dispersal between patches may not be possible in highly fragmented landscapes due to physical barriers to movement. Shifting range in response to climate change requires suitable new habitats to be accessible, and for the required traveling distances to be within the capacity of the species that is shifting range. In particular, "responses to climate change have been observed across many species. There is a general trend for species to shift their ranges poleward or up in elevation. Not all species, however, can make such shifts, and these species might experience more rapid declines. Many species will be unable to track suitable climates under mid- and high-range rates of climate change during the 21st century (medium confidence). Lower rates of change will pose fewer problems. Some species will adapt to new climates. Those that cannot adapt sufficiently fast will decrease in abundance or go extinct in part or all of their ranges." (see http://www.torreyaguardians.org/assisted-migration.html).

ADAPTIVE RESPONSE

Evolutionary adaptation, or simply adaptation, is the adjustment of organisms to their environment in order to improve their chances at survival in that environment. Living organisms can adapt to changes in their living environment via two major processes: genetic evolution and/or phenotypic plasticity.

Longitudinal studies of wild populations provide the opportunity to determine whether phenotypic changes are adaptive or not. A phenotypic change qualifies as an adaptive response to climate change if three conditions are met:

• a climatic factor changes over time,

• this climatic factor affects a phenotypic trait of a species,

• the corresponding trait change confers fitness benefits.

MICROEVOLUTION

"Adaptation through genetic evolution is achieved by modifying, between generations, the genetic composition of the population via natural selection. For example, mosquitoes carrying a new mutation that appeared in the 1980s have a much better survival rate against insecticides than other individuals not carrying this genetic innovation. As a result, this mutation and the insecticide resistance it provides spread through natural mosquito populations in about two decades. This process of adaptation through changes in genetic composition requires that the selected traits are at least partially transmissible between generations, from parent to child." (see https://www.sorbonne-universite.fr/en/news/understanding-mechanisms-adapting-climate-change).

Natural Selection can shift allele frequencies in one of three ways:

• Stabilizing selection favors the average or mean value for a trait and selects against the extremes.

• Directional selection favors one extreme over the other, can be either the lower or upper extreme.

• Diversifying selection (sometimes called disruptive selection) favors the extremes, and selects against the middle or average.

The ability to genetically adapt through microevolution hinges on the availability of standing genetic variation on which natural selection can act. It is important to note that since genetic changes take place between generations, genetic evolution is all the more rapid the shorter the generation time of the species.

• Adaptation over evolutionary time scales (thousands to millions of years) can occur by the generation of beneficial traits by gradual genomic changes ranging from whole genome duplications to point mutations.

• Adaptation on ecological time scales (tens to hundreds of years), in contrast, requires adaptive genetic variation to already be available prior to the environmental shift, clearly presenting a challenge for adaptation to novelty on ecological timescales. This challenge can be overcome by species with large population sizes and short generation times, such as some arthropods, marine species, microbes, and plants, because adaptive mutations arise more frequently, and are less likely to be lost due to demographic changes. Evolutionary responses that track such novel and changing environments were shown for instance in bacteria with the evolution of antibiotic resistance and in insects with pesticide resistance (Palumbi 2001). We have also witnessed the evolution of the color in a common butterfly following the blackening of tree bark due to heavy air pollution in England in the 19th century.

But human-mediated ecological changes are nowadays often so rapid that evolutionary processes may simply be unable to keep pace with the changes that are taking place. The rate of current environmental change exceeds the evolutionary response rate of many populations (Bell & Collins 2008; Chevin et al. 2010; Hoffmann & Sgro 2011). In particular, for many species, the reproductive rates of species are too slow, the generation time too long, or the population size is too small to result in rapid evolutionary responses (Lande 1998; Reznick & Ghalambor 2001; Bell & Gonzalez 2009).

PHENOTYPIC PLASTICITY

Phenotypic plasticity is thus likely to represent the first response of individual organisms to rapid human-induced environmental changes. Phenotypic plasticity occurs when the phenotype expressed by a genotype varies across a range of environments. It can take place through phenology, developmental plasticity, physiological adjustments and behavioral flexibility.

As explained in https://www.sorbonne-universite.fr/en/news/understanding-mechanisms-adapting-climate-change: "While genetic adaptation is a process that induces changes between generations in a given population, phenotypic plasticity is an adaptation process that can induce changes within each individual in the population. For example, in many mammals, the amount of adipose tissue in an individual can vary according to several environmental parameters, such as cold weather. Similarly, many species increase their alertness time when the risk of predation is high. Plasticity is therefore expressed within a generation, making it possible to adapt more rapidly than through genetic evolution. In particular, it allows the organism to readjust in response to changing environmental conditions over the course of an individual's life. Often, organisms need time to be ready for new environmental conditions; if the plastic response is the development of a defense against predators, this must be put in place well before the encounter with the predator. Organisms therefore use clues present in the environment to develop the right response at the right time. This is the case for tadpoles who develop different morphologies depending on the presence or absence of predator odor. In the current context, the existence of a mechanism such as phenotypic plasticity, which is widespread and can allow very rapid adaptation to environmental changes, is of major interest for understanding and anticipating the consequences of anthropogenic upheavals of biodiversity."

Phenotypic plasticity results from inherited epigenetic changes, that is phenotype changes that do not involve alterations in the DNA sequence but rather regulation of gene expression (e.g., via DNA methylation or Histone modifications).

For a continuous phenotype responding to a continuous environment, the concept of plasticity is captured by the slope of the reaction norm relating phenotype to environment. The reaction norm of a trait describes the range of phenotypes expressed by a genotype along an environmental gradient. As explained in Chevin et al. 2012: "Some traits are flexible (or ‘labile’) and respond to the environment throughout lifetime (notably learning and other behavioural traits). Others are ‘fixed’, and take only one value during lifetime, set by the environment experienced at a critical point during development (mostly morphological traits). In between are traits that are repeated on discrete occurrences during lifetime, such as yearly breeding dates of birds and mammals, or annual growth rings of trees, which allow measurement of plasticity on individuals instead of genotypes/families (Nussey, Wilson & Brommer 2007)." Selection on plasticity requires that individual variation in the response to the environment (IxE; Nussey et al. 2007) exists.

Phenotypic plasticity has often been seen primarily as an alternative to genetic divergence and a constraint on adaptive evolution, making populations less responsive to natural selection. However, phenotypically plastic traits can promote adaptive evolution and the origin of species (Fitzpatrick 2012).

Fitzpatrick (2012) thus distinguished 3 types of phenotypic plasticity:

• adaptive plasticity, which is thus a tendency for a genotype to express a phenotype that enhances its ability to survive and reproduce in each environment.

• nonadaptive plasticity, which includes any response to environmental induction that does not enhance fitness (including maladaptive responses).

• noisy plasticity, which is effectively unpredictable phenotypic variation owing, for example, to developmental instability or random perturbations within environments.

Adaptive phenotypic plasticity can facilitate colonization of new niches and rapid divergent evolution. Non-adaptive plasticity too can interact with selection to promote or inhibit genetic differentiation. Phenotypic plasticity of reproductive characters might directly influence evolution of reproductive isolation and cause assortative mating.

BEHAVIOURAL PLASTICITY

The initial response of individuals to human-induced environmental changes is most often behavioural plasticity, that is a change in an organism's behavior that results from exposure to stimuli, such as changing environmental conditions. Behaviours are indeed one of the most plastic components of the individual phenotype. They can indeed change more rapidly in response to changes in internal or external stimuli than is the case for most morphological traits and many physiological traits. Behvioural plasticity facilitates adjusting to changing environments. It is expected to be favored by selection when environments are variable and when the benefits of accurately assessing environmental state outweigh the costs (DeWitt et al. 1998). Behavioral plasticity may differ between individuals (Wolf et al. 2008; Dingemanse and Wolf 2013).

Thanks to the high reactivity and high lability of behaviours, behaviors may play a key role in species response and adaptation to human-induced rapid environmental changes by allowing animals to adjust behavior to suit the conditions of its immediate environment (Charmantier et al. 2008; Sih et al 2011; Tuomainen & Candolin 2011; Candolin & Wong 2012, Sih 2013). This rapid response can improve the performance of individuals subjected to large and sudden disturbances and maintain viable populations. It can also provide additional time for genetic changes to take place, thus facilitating adaptation to new conditions. Behaviour may thus help explain why some species are able to survive and even thrive in human-modified environments, while others are on the brink of extinction as a result of the same changes. However, behavioural plasticity is not always sufficient to cope with Human Induced Rapid Environmental Changes.

As Snell-Rood (2013) and (Schausberger et. 2018) explained, "Behavioural plasticity can be broadly classified into two types:

• Developmental behavioural plasticity corresponds to the traditional definition of phenotypic plasticity, where a genotype expresses different behavioural phenotypes in different environments as a result of different developmental trajectories triggered by those environments. Developmental behavioural plasticity encompasses all of what is generally defined as learning’ or any change in the nervous system as a result of experience. However, developmental behavioural plasticity also includes developmental changes in morphology and physiology relevant to a particular behaviour, such as changes in muscles, limbs or bones that influence foraging or locomotion (e.g. Wainwright et al. 1991; Losos et al. 2000; Young & Badyaev 2010)."

• "Activational plasticity refers to immediate behavioural changes, with the underlying neural network being already present; developmental plasticity refers to time-lagged behavioural changes following experience, because of the time needed to establish the underlying neural network and to consolidate memory of a given experience."

"Activational plasticity allows immediate contextual behavioural changes, whereas developmental plasticity is characterized by time-lagged changes based on memory of previous experiences (learning)" (Schausberger et. 2018)."

According to Snell-Rood (2013): "Biologists have long been interested in understanding why phenotypic plasticity varies within and between species, a question which often comes down to understanding costs and benefits of plasticity. The costs of developmental behavioural plasticity stem from the fact that much of this form of plasticity is underlain by ‘trial-and-error’ or developmental selection processes. Developmental or somatic selection involves both sampling of a range of phenotypes and environmental feedback on which phenotypes perform well in current conditions (West-Eberhard 2003; Snell-Rood 2012). Sampling, whether exploring resources, the environment or a range of phenotypes, requires time, energy and necessitates making mistakes (Laverty & Plowright 1988; Ericsson et al. 1993; Janz & Nylin 1997; Byers et al. 2005), referred to as the cost of naiveté (Dukas 1998), or the exploration-exploitation trade-off (Kaelbling et al.1996).

Both types of behavioural plasticity impact evolution in novel environments by increasing the probability of survival in that environment. Developmental behavioural plasticity is particularly relevant to survival in novel environments because trial-and-error processes such as learning, which include both phenotype sampling and environmental feedback, have the ability to immediately shift an entire population close to a novel adaptive peak (Hinton & Nolan 1987; Snell-Rood 2012). Such plasticity can result in the development of alternate phenotypes that differ in morphology, behaviour and physiology. Activational behavioural plasticity is also important for survival in new environments because it can allow immediate adjustment to novel environments. For example, stringent preferences for mates or resources are often adjusted when resources or mates are less common. Mate preferences are often relaxed when organisms are reared in low-density environments (Bailey & Zuk 2008; owler-Finn & Rodriguez 2012), which might facilitate survival of populations in new environments where population density is low. Thus, plasticity in acceptance thresholds based on environmental conditions represents differential development of activational behavioural plasticity that may facilitate survival in new environments.

Behavioural plasticity, in particular developmental plasticity, also has major impacts on evolutionary diversification (Price et al. 2003; West-Eberhard 2003; Lande 2009; Pfennig et al. 2010). Plastic populations have the potential to immediately shift to new adaptive peaks, especially if phenotypes develop through learning-like processes that incorporate both sampling and environmental feedback (Hinton & Nolan 1987; Frank 1996, 2011; Snell-Rood 2012). Once on these new selective peaks, the costs of plasticity, which are especially pronounced for learning and similar mechanisms of plasticity, should select for more efficient production of the phenotype; in other words, reduced plasticity. Alternatively, if the environment is still variable, there may be selection for habitat choice, followed by reduced plasticity. Either way, genetic assimilation may result, where an initially environmentally induced phenotype is constitutively produced, potentially leading to diversification (see Pigliucci & Murren 2003; West-Eberhard 2003; Pfennig et al. 2010; Bateson & Gluckman 2011). Because developmental plasticity can simultaneously affect the development of behaviour, ornaments and sensory systems, it may be especially important for diversification because it can lead to immediate prezygotic isolation. It is well established that the environment affects the development of signals: song structure is often learned (Marler 1997; Doupe & Kuhl 1999) and then adjusted in noisy environments (Gross et al. 2010; Luther & Derryberry 2012), and the development of ornamentation often depends on diet (Hill 1992; Toomey & McGraw 2009). We also know that the development of sensory systems depends on the environment. For instance, visual systems develop quite differently in different lighting conditions (Cronin et al. 2001; Fuller et al. 2010). This suggests that there may be simultaneous developmental shifts in traits that affect survival in a novel environment and traits that affect mate choice."

Behavioural response to human-induced rapid environmental change fall into several main categories (Sih et al. 2011):

(i) avoiding or coping with novel enemies (e.g. predators, parasites, diseases; including humans);

(ii) adopting and utilizing novel resources or habitats;

(iii) avoiding or coping with novel abiotic stressors (e.g. pollutants);

(iv) adjusting to changing spatiotemporal conditions (e.g. habitat fragmentation, climate change).

Some individuals or species exhibit maladaptive responses that can have serious detrimental consequences, while others show interestingly ‘adaptive’ responses despite the fact that human-induced rapid environmental change is putting them into evolutionarily novel conditions.

Personality

In the context of rapid environmental change due to human activities, the ability of individuals in a population to adapt and thrive in a new environment may depend on their ability to cope with fluctuations in their environment through the expression of individual behavioural flexibility. It is therefore important to assess the extent to which different behaviors are predictable and what factors influence their level of consistency.

Animal personality (also called temperament or type of behaviour) describes the differences in consistent individual behaviour and repeatable over time and over context (Spiegel et al., 2016).

As explained by Westneat et al. (2011): "Broadly speaking, the proportion of total variance in phenotype that is between-individual is repeatability (e.g., Lessells and Boag 1987; Falconer 1989). Despite its apparent flexibility, behavior can exhibit considerable repeatability (e.g., Bell et al. 2009). As applied to behavior alone, repeatability has been called “personality” (e.g., Réale et al. 2010). Consistent individual differences in behavior are now reported across different animal taxa (e.g., Clark and Ehlinger 1987;Dall et al. 2004; Sih et al. 2004)."

Personality traits of individuals commonly studied in ecology include boldness, aggression, or sociality (Andrew Sih et al., 2004; Andrew Sih & Del Giudice, 2012). These traits are often correlated with each other, leading to behavioural syndromes, e.g., individuals who are bolder in the presence of predators are also more aggressive towards conspectives. The personality of animals can have a significant impact on their adaptive value. Some personality types may be more adapted to particular environmental contexts.

As explained by Westneat et al. (2011): "In many animal taxa, behavior varies both among individuals (animal “personalities”) and within individuals (“plasticity”). Personality and plasticity may co-vary if individuals differ in responsiveness to changes in their environment (“I × E” interaction). The relationship between personality and plasticity is important as the two concepts describe variation at two different levels, but the linkage between them has had a confusing history. On the one hand, Sih et al. (2004) suggested that personality represents non adaptive limits to plasticity. Others have conflated personality and plasticity by labeling differences in plastic responses within populations as personality (e.g., responsiveness, ClarkI 1991; coping styles, Koolhaas et al. 1999; Coppens et al.2010; reactivity, Wolf et al. 2007; inconsistency, Royle etal. 2010). Moreover, operational measures of personality and plasticity are not always distinct. Consistent differences between individuals may appear to exist if plasticity exists but some individuals experience a different subset of environments than others (e.g., Martin and Re ́ ale 2008; van de Pol and Wright 2009). Plasticity could also occlude personality if it contributes to within-individual variance that masks between-individual differences. These issues suggest that clear statistical definitions of plasticity and personality (e.g., Dingemanse et al. 2010) could help clarify the ways in which they each contribute to variation in behavior and help link within- and between-individual patterns of variation."

As explained in Hall et al. (2016): "Theory suggests that consistent behavioral differences among individuals (“personalities”) may select for individual differences in behavioral plasticity, and vice-versa, in a frequency-dependent coevolutionary process (McNamara et al. 2009; Wolf et al. 2011). Thus individuals that behave flexibly in a social context could experience fitness benefits when interacting with individuals that show predictable behavioral differences, and vice-versa. For example, if some individuals differ predictably in aggressiveness, others could benefit by adjusting their probability of attack according to the level of aggression of their rival. A better understanding of individual differences in behavioral plasticity in fitness-relevant contexts is necessary to determine the adaptability of individuals to changing environments."

CONSEQUENCES OF BEHAVIOURAL RESPONSES

The behavioural responses of animal species to environmental changes (e.g. in terms of movement, activities and feeding) can affect not only population dynamics and genetics, but also the strength and nature of interactions between species, for example by altering the spatio-temporal distribution of different species or the respective sizes of their populations. These changes in the structure and dynamics of biodiversity can in turn have important consequences on the structure, functioning and stability of ecosystems.

The behavioural responses of species to environmental changes can also directly affect the functioning of ecosystems, where these organisms (e.g. pollinators, decomposers, herbivores) play a key role in the functioning of ecosystems (e.g. nutrient flow, litter decomposition, pollination), as well as ecosystem services.

“We have only a basic understanding of how behavioral responses in one species, through its effects on others, might alter ecosystem processes” (Wong & Candolin 2014).

In this context, I am interested in the following questions:

• How do behaviours vary within individuals, between individuals within populations, and between populations or species?

• What are the proximal and ultimate factors responsible of these variations?

• What are the respective roles of environmental effects (phenotypic plasticity) and genetic effects (microevolution) in the variability of behavioral traits?

• What are the impacts of environmental changes on behaviors?

• Are these behavioural changes adaptive?

• What are the consequences of these variations in terms of fitness, genetic diversity and population dynamics?

• Whats are the cascading effects of behavioural changes in terms of ecosystem functioning and ecosystem services?

Sexual selection and evolution of mating systems

Roe deer project

My doctoral research (2003-2007) at CEFS-INRA and Grimsö Wildlife Research Station (Sweden), under the co-direction of Mark Hewison and Henrik Andrén, focused on sexual selection and mating system of European roe deer (Capreolus capreolus). My work was based on the combined use of molecular tools, longitudinal capture-mark-recapture data and field ecology data within 3 contrasting populations monitored over the long term in Europe. I established a close collaboration with Jean-François Cosson and Maxime Galan from CBGP-INRA to genotype several thousand of samples on 22 microsatellite markers.

Using paternity analyses, I provided the first estimates of reproductive success in males and showed the existence of a low opportunity for sexual selection in this species in relation to its low degree of sexual size dimorphism (Vanpé et al. 2008 Behav Ecol). I also showed that multiple paternity was possible but quite rare in deer, and may have evolved as an inbreeding avoidance strategy (Vanpé et al. 2009 Biol J Linn Soc). I identified the main factors determining variations in male reproductive success: age, body mass, antler size, territory size (Vanpé et al. 2009 J Mamm, Vanpé et al. 2009 J Anim Ecol, Vanpé et al. 2010 Oikos). Finally, I showed that antler size of males was highly correlated with age and body mass, but appeared to be little affected by environmental conditions, suggesting that it is an honest signal of male phenotypic quality, which could be used by females when choosing a mate or by other males as an indicator of the strength and fighting ability of rival males (Vanpé et al. 2007 Am Nat).

From April 2016 to January 2017, I pursued this research in the framework of my postdoctoral fellowship at the LBBE-CNRS within the AGEX ANR project, taking advantage of the massive genotyping performed during my PATCH ANR project on various roe deer populations in France and Sweden in collaboration with CBGP-INRA. This project aimed at evaluating how the age of the partners in roe deer influence multiple parentage and paternity, and how the paternities are spatially distributed to see if females reproduce with neighboring males or more distant males.

I showed that mating between old females and prime-aged males was more frequent than mating between prime-aged females and prime-aged males, which suggest that old females avoid old mates (Vanpé et al. 2019 Biol J Linn Soc).

I also extended this research to the study of sexual selection in large mammals using a comparative approach. J-F. Lemaître (postdoctoral fellow in the framework of my PATCH ANR project) showed the existence of a non-linear allometry between antler length and body mass in deer (Lemaître et al. 2014, Lemaître et al. 2015 Biol Letters).

I also showed that there was a positive correlation between sexual dimorphism of body size and body mass (Rensch's rule) in large mammals in general and in Artiodactyls and Diprotodonts (but not in Primates and Pinnipeds) (Vanpé et al. Submitted to Am Nat). This study reveals for the first time the major role of sexual selection in the evolution of sexual size dimorphism in large mammals, through the advantage of large sizes in males in inter- and intra-sexual competition for access to females, but also the agility of males in Primates and Pinnipeds breeding in 3D habitats.

Understanding the evolutionary and ecological mechanisms behind phenotypic responses to landscape change, and in particular whether these responses are adaptive or not, and genetically or environmentally induced, is an important challenge for evolutionary ecology. I have been closely contributing since 2015 to an innovative project of the dpt. EFPA of INRA that I co-funded with my ANR PATCH, and which is coordinated by Erwan Quéméré (CEFS-INRA)? This project aimed at developing SNP markers densely distributed in the roe deer genome in order to accurately measure the level of kinship between each pair of individuals as well as the inbreeding rate of populations, and to have better estimates of quantitative genetic parameters.

We were able to study the influence of environmental conditions on the evolution of body mass in two contrasting roe deer populations, by reconstructing the multi-generational pedigree of these populations from microsatellite genotyping data and using a quantitative genetic approach (Animal Model) (Quéméré et al. 2018 BMC Evol Biol). We found that the level of additive genetic variance for body mass was very sensitive to environmental conditions and could vary greatly within and between populations depending on the availability of resources during early fawn growth. On the other hand, maternal genetic variance of juvenile body mass was not detectable for cohorts that experienced poor environmental conditions, but increased markedly when rearing conditions were better.

The perspectives are now to study the genetic determinism of other morphological (antler size, body size), behavioural (personality) and life history (senescence, phenology) traits in contrasting roe deer populations in order to study the phenotypic response of roe deer to global changes.

Echidna project

I have brought my expertise in spatial analysis and molecular ecology for 2 months in 2008 as a guest researcher on a research project from the University of Tasmania (Australia) led by Stewart Nicol. This project aimed at using molecular tools in combination with modern field techniques in ecology (GPS and VHF transmitters, transponders) and physiology (ultrasound, sperm study, temperature sensors) to study spatial ecology, reproductive tactics and sexual selection within a population of short-nosed echidnas (Tachyglossus aculeatus).

The monotremes, which not only exhibit original characteristics (e.g. oviparity) but also characteristics typical of metathereal and eutherian reptiles, birds and mammals, represent a unique order within mammals that diverged from the other orders about 200 million years ago and thus provide a unique study model for understanding evolutionary processes in mammals. However, their reproductive tactics remain poorly understood.

We showed that despite a rather solitary behavior and the absence of sexual dimorphism in the short-nosed echidna, both sexes are promiscuous, the home range of males is larger than that of females, and the degree of overlap of home ranges between individuals is significant. We also related variations in internal temperature of females to their activities (hibernation, mating, lactation) and demonstrated the existence of excursions in females during the rut in which they mate with males in breeding groups (Nicol et al. 2011 J Mamm).

Evolution of social organization and dispersal

Wombat project

Although common wombats (Vombatus ursinus, marsupial) are considered as solitary because they do not live in groups and feed in isolation, they may share their burrows with other conspecifics, although rarely at the same time. They may therefore have developed a subtle form of sociality related to burrow sharing. Furthermore, although dispersal is typically biased in favour of males in mammals, wombats show a biased dispersal in favour of females, which may have evolved in relation to burrow use.

The ultimate goal of my 6-month postdoctoral fellowship at the University of Queensland (Australia) in 2009-2010 in Anne Goldizen's group was therefore to study the influence of burrow use and sharing on the evolution of sociality and female-biased dispersal in common wombats. More specifically, I used a non-invasive genetic approach (hair traps) to study the patterns of burrow sharing among individuals, characterize the social network, study the role of the degree of kinship in burrow sharing and test the existence of a biased dispersal in favour of females. I showed (results presented at the Socior conference in Paimpont in 2010 and TiBE in Porto in 2011) that the same burrow could be used by up to 6 different individuals and that males play a central role in the social network. Furthermore, while in females, the degree of kinship between individuals sharing a burrow was much higher than between individuals not sharing a burrow, there was no significant difference in males, suggesting the existence of a biased dispersal in favour of females.

Roe deer project

I also studied the proximal and ultimate factors responsible for natal dispersal and excursions of females roe deer through collaborations during my PhD at CEFS-INRA (2003-2007) and my PATCH ANR project (2012-2015). We characterized the existence of female rutting excursions in various roe deer populations and suggested a link between this behaviour and inbreeding avoidance (Richard et al. 2008 Behav Processes; Debeffe et al. 2014 Oecologia). We showed the absence of density dependence in natal dispersal in roe deer (Gaillard et al. 2008 Proc R Soc Lond B) and highlighted the existence of a dispersal syndrome in this species, demonstrating that future dispersing individuals were less neophobic and had higher energy budgets than future philopatric individuals (Debeffe et al. 2014 Proc R Soc Lond B). Finally, I was able to show that the degree of individual heterozygosity at immunogenetic but not microsatellite markers had an effect on roe deer dispersal rate (Vanpé et al. 2015 Oecologia, Vanpé et al. 2016 Oikos). This was the first time to our knowledge that a study demonstrated a link between diversity of immunogenetic markers and dispersal.

Personality

Roe deer project

We have shown that docility in roe deer was as repeatable in the short term as in the long term and that repeatability did not differ significantly according to the age and sex of the individuals (Debeffe et al. 2015 Anim Behav). Finally, individual variation in repeatability of docility was not correlated with individual body mass.

We distinguished 2 main personality types related to the docility of animals: proactive individuals are more mobile and aggressive in the face of stress, while reactive individuals are more passive and react less in difficult contexts. We have shown that the fawns of proactive dams survived better in open agricultural habitats, whereas the fawns of reactive dams survived better in forest habitats in roe deer (Monestier et al. 2015 Behav. Ecol.).

An animal's flight behavior is a reliable indicator of the risk it perceives in its environment and has thus been widely used to assess how prey cope with anthropogenic disturbances. In the context of the landscape of fear, we have thus studied the behavioural plasticity of roe deer in their response in terms of flight behaviour to perceived spatio-temporal variations in risk (in terms of landscape openness, proximity of human infrastructure and hunting presence) and reward (in terms of habitat quality) within a fragmented agricultural landscape (Aurignac). We found that the flight behavior of deer in the face of danger varied according to the degree of openness of the landscape, the hunting season, the proximity of roads and the quality of habitat (Bonnot et al. 2017 to Anim Behav).