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Effect of environment on sexual selection
Environment may vary across time (Chaine & Lyon, 2008; Kasumovic, Bruce, Andrade, & Herberstein, 2008) and across space (spatial heterogeneity), and may act at different spatial scales: environment can differ between populations that are geographically isolated, but it can also display heterogeneity at local scale thereby proposing a range of ecological variation within populations (Jann, Blanckenhorn, & Ward, 2000). Environment is known to be the main agent of natural selection. It first acts through processes not linked to sexual selection, such as survival until reproduction. However, this selection will potentially affect phenotypic availability for subsequent reproduction. Second, environment will also influence growth and metabolic status of individuals, conditioning their future reproductive investment. The environment can also influence sexual selection directly, by biasing adult sex ratio in the population (due to differential mortality), by biasing local operational sex ratio (spatial heterogeneity of sex distribution in the population), by changing costs and benefits of mating tactics (Head, Wong, & Brooks, 2010), or by changing the relationship between mates phenotype and offspring survival, therefore changing the benefits of mate choice.
While it seems intuitively logical that costs and benefits can be environment dependent, it has also been formally described in analytical models. Kokko & Jennions (2008) assume that selective pressures influence individual tactics by acting differentially on costs outside and inside the mating pool (differential mortality of rate), and that an optimal strategy within a population can be found where all individuals of both sexes achieve maximal fitness. They also show that the benefits inside the mating pool depend on OSR (Table 1), Adult Sex Ratio (ratio of number of mature males on number of mature females in a population at any time, ASR) and survival of individuals. Therefore survival and reproductive success in each group (inside and outside of the mating pool) govern sexual selection. It is predicted that if survival changes (in or out of the mating pool) for one of the sexes, then the evolutionary equilibrium that describes the optimal strategy for both sexes changes. Kokko and Jennions (2008) predict that evolution of sex roles relies on a tradeoff between 1) providing parental care and being no longer available for mating, and 2) avoiding parental care, therefore staying in the mating pool to improve mating prospects. Therefore, mortality rate – which is generally highly environment dependent-, OSR and ASR (that represent social and demographic environment) may lead to the evolution of sexual selection.
Can human induced environmental change affect sexual selection?
Many studies have demonstrated that human induced global change can act on ecological processes (Kerley et al., 2002; Relyea, 2001). A good example is provided by the effects of the alteration of climatic patterns in recent decades (IPCC 2013) that have dramatically shifted the migration dates in birds therefore affecting phenology in these species (reviewed in Gordo, 2007). Several studies showed for example that increase in temperatures may affect food availability reducing chicks survival and therefore have direct consequences on population size (Both, Bouwhuis, Lessells, & Visser, 2006). Additionally, temperatures may have considerable effect on sex ratio at hatching or birth in species with environment-sex determination depending on temperature. Urbanization, deforestation and habitat fragmentation are other examples that may lead to different behavioural responses that will condition population dynamics, evolutionary processes and ultimately biodiversity. Specific causes of behavioural responses can be multiple (ie. inducing changes in the sensory environment, changes in habitat size, habitat structure and connectivity and changes in density of conspecific). Increases of temperature and global change more generally can affect individual (offspring and parents) survival (Angilletta Jr, Niewiarowski, Dunham, Leaché, & Porter, 2004; Hance, van Baaren, Vernon, & Boivin, 2007), and reproductive output (Winkler, Dunn, & McCulloch, 2002). While a lot of focuses on the consequences of human induced changes on survival and individual status, far less work has been devoted to study their consequences on sexual selection (Blanckenhorn, Stillwell, Young, Fox, & Ashton, 2006; Moller, 2004). For example, plastic behavioural responses can influence mating patterns and physiological processes (reviewed in Tuomainen & Candolin, 2011). For instance, alterations in mating behaviour and mate choosiness can for example affect gene flow between populations and generate reproductive isolation as seen in cichlids (Maan, Seehausen, & Van Alphen, 2010; Seehausen, 1997). Likewise, in sticklebacks, eutrophication in the Baltic Sea increases growth of algae, which in turn increases the time and energy spent by sticklebacks on courtship and mate choice: this variation in energy budget has direct consequences on the cost of mating (Candolin, Salesto, & Evers, 2007). The effects of human-induced environmental change can therefore also directly affect sexual selection.
Brown trout, sexual selection, and environmental variation
Darwin (1871) often reflected on salmonid astonishing life histories, either because of their life cycles, or because of their intersexual differences in traits behavior or phenotypical traits. Salmonid fishes are indeed an appropriate system for studying evolution of sexual selection facing environmental conditions. First, they are renowned for their tendency to show a wide range of variable behaviours during reproduction and these behaviours can be now be measured in natural and or experimental environments (Esteve, 2005; Freychet, 2011; E Petersson, Järvi, Olsén, Mayer, & Hedenskog, 1999; Schroder, 1981). Second, in salmonids, the environment can vary spatially and temporally leading to a possible evolution of costs and benefits of reproductive strategies which are closely linked with biotic and abiotic pressures.
The genus Salmo is one of the most studied within the family of Salmonidae, along with Salvelinus and Oncorhynchus. The salmonid subfamily Salmoninae exhibits about 30 species well described in the literature (Klemetsen et al., 2003). In the present manuscript I will describe only Salmo trutta L. (brown trout), because I used it as a case study throughout my thesis project. Brown trout is indigenous to Europe, North Africa and western Asia (Klemetsen et al., 2003). Brown trout is present in many regions of Europe from north of Iceland, Scandinavia and Russia to South of the Mediterranean Sea. After many introductions, brown trout has now reached a world-wide distribution (Elliott, 1994) because of its impressive capacity to spread and colonize new areas with ecological variability (Lecomte, Beall, Chat, Davaine, & Gaudin, 2013). Salmo trutta is defined as an anadromous fish which can have two reproductive strategies: the migratory strategy and the resident strategy. In the former, juveniles migrate to the sea to maturate with a period of smoltification and come back to their birth river or a different river for spawning (respectively “homing” and “straying”), whereas residents trout perform both their development and reproduction period in river: the present manuscript will focus only on resident brown trout. Accordingly, river connectivity can affect dispersal in this species and environmental contrast varies greatly from upstream mountain torrents to lowland plain rivers. Thus, local conditions such as population density, ASR, OSR and phenotypic distribution may be strongly affected by these environmental contrasts.
In brown trout, females compete for spawning sites and spawn on gravel bars where they excavate a series of depressions called “nests” where they lay their eggs (Greeley, 1932). The availability of these spawning sites is structured by the variation of particle size. Particle size can notably condition oxygen availability in the redd (Acolas, 2008) and can provide a good protection for the eggs. To access females, a fierce competition between males occurs with a display of agonistic behaviours, such as chases, bites and lateral display (Keenleyside & Dupuis, 1988). Interactions between males are often hierarchized as a function of their reproductive status, i.e. dominant or peripheral (Blanchfield & Ridgway, 1999; Erik Petersson & Järvi, 2001). Larger males have been described as more advantaged in comparison with smaller males during contest competition in different species of salmonids (Fleming & Gross, 1994; Schroder, 1981). Females have been reported to exhibit preference for adiposis fin size (Petersson et al., 1999) and for relative individual body size (Labonne et al., 2009). As a result of strong preference and competition, sexual selection is expected to be relatively strong in brown trout, and recent analyses confirm this view, while also mentioning the role of environmental uncertainty in the maintenance of plasticity in sexual behaviours (Serbezov et al., 2010). Although this thesis will not focus on the genetic basis of traits involved in sexual selection, it is of interest to note that the salmonid genome underwent a polyploidy event some tens of millions years ago (Allendorf & Thorgaard, 1984; Hoegg, Brinkmann, Taylor, & Meyer, 2004), and that the current genome might be highly influenced by this event: former copies of genes may have evolved to code for different functions, whereas some others may still code for similar functions. Second, this polyploidy event de facto erased the sex chromosome. Recent research suggest that a Sex locus is now present in many salmonid species, but at various stage of degradation, and very little is currently known regarding the genes that might be physically linked to this locus (Yano et al., 2012, 2013).
Environmental change and brown trout reproduction
In addition to changes in land use, water use and river channelization that may affect the brown trout life cycle at various stages and levels, the effects of climate change since the late 19th century (IPCC 2013) also threatens river ecosystems. This is particularly theoretical models predict an increase of the rainfall perturbation in frequence and intensity (Dankers & Feyen, 2008; Milly, Dunne, & Vecchia, 2005; R. J. Stevenson & Sabater, 2010; Vitousek, 1994). Indeed the increase in the frequency of extreme rainfall events is expected to directly influence water discharge in rivers, thereby potentially affecting the suitability of reproduction habitats for brown trout. Stream flow is predicted to increase in the western areas of Europe (Stahl et al., 2010; Stahl, Tallaksen, Hannaford, & van Lanen, 2012) such as in the Pyrénées mountain range. Moreover an increase of water temperature in rivers is also predicted with an increase of air temperature (IPCC 2013) which can affect metabolic rate of individuals and therefore their allocation in biological activities such as reproduction (Charnov & Gillooly, 2004; Gillooly, Brown, West, Savage, & Charnov, 2001).
An increase of water discharge may have direct consequences on resource availability especially in freshwater food webs (Perkins, Reiss, Yvon-Durocher, & Woodward, 2010). Therefore energy stores are affected which will in turn modify the allocation of energy to the different functions (e.g. reproduction, survival, maintenance…) and will ultimately modify condition survival. This would in turn shuffle the initial conditions at the onset of reproductive season, by changing density, ASR and OSR of populations. Increased stochasticity in river water flow could also impact the energetic budget of spawners during reproduction, by impacting directly the cost of competition or parental care. Droughts and large floods may also have direct impacts on habitat structure. They may impact significantly survival in redds which, by providing protection against predation for the embryonic stage, are at the center of this species’ reproductive system and life cycle. Because the adaptive value of behaviours associated to sexual selection mechanisms is modulated by offspring survival, the evolution of reproductive system in brown trout is probably linked to variations in selective pressures on offspring viability.
For all these reasons, it is logical in this thesis to investigate the evolution of populations and sexual selection in relationship with environmental change, and specifically with climate change.
How to read this manuscript
The general objective of this work is to investigate the effects of environment (at different scales) on the evolution of sexual selection in brown trout, to better understand how environmental factors can shape the evolution of traits and behavioral responses. Environment was therefore considered at different scales: 1) individual scale 2) inter-individual scale, taking into consideration phenotypic traits of sexual partners 3) inter-population scales. To address those scales, two groups of experiments were designed: in natural and in semi natural conditions, which is a prerequisite to measure effects of selection in a realistic context. I also developed specific experimental and statistical methods to improve the measure of reproductive investment and to increase our insight into fundamental components of sexual selection such as mating success. Using these new methods, as well as the general background of behavioural and evolutionary ecology, I then studied the effects of environmental variation on the costs and benefits of each individual strategy involved in reproduction. I particularly focused on one expected trend in environmental modification: increased stochasticity of water flow.
The present manuscript is composed of six chapters, the first one being this introduction. The second chapter describes the different experiments conducted in order to answer to the general objectives of this thesis. The reader will also find there some technical developments regarding several aspects such as the measure of reproductive investment. Often, in the following chapters, references will be made to this methodological chapter. Sometimes though, methodological details will be revealed later in each chapter, because they do not concern the whole document. This should avoid unnecessary page browsing. The third chapter is based on an experiment and describes how individual status affects components of sexual selection. This individual status is investigated through traits, such as weight and its variation, but also through metabolic condition (as revealed by the study of energetic metabolites dynamics in the plasma) over the reproductive season, or behavioural activity during reproduction. The fourth chapter will then replace the individual in its social context: I will there investigate interactions between individuals, as seen by OSR and phenotypic availability variation, for instance, and some aspects of intra-sexual competition. A special focus will then be made on the fundamental dependency between sexual partners to analyse mating and reproductive success, and to that end, I will propose a new statistical model to decompose sexual selection stages, account for phenotypes of both sexual partners, and improve the use of various source of data in a unified framework. I will also propose a comparison with the classical approaches to estimate selection gradients in sexual selection. The fifth chapter will bring environment into action, benefiting from the previous chapters and developments to improve our grasp on environment effects on sexual selection. I will here study how environmental stochasticity may affect post-zygotic selection through habitat selection by females and how environmental stochasticity may condition reproductive investment, mating success, and reproductive success. These multiple potential effects of environmental stochasticity will each time be investigated in two populations, in order to check if environmental variation has a uniform impact on populations, or if each population may react differently to this selective pressure. I also placed individuals originating from different populations in sympatry, which will allowed testing reproductive isolation (and therefore gene flow) due to sexual selection between populations, depending on environmental contrast (here, the stochasticity of environment).
In each of these five chapters, some elements of discussion will be provided. The last and sixth chapter proposes a more general discussion. Here, I will then try to synthesize my findings, review the progresses made and the obstacles encountered, point at areas where more investigation is needed, and finally provide a general perspective for the effect of environment on sexual selection in brown trout.
Table of contents :
CHAPTER I: INTRODUCTION
I. A general background for sexual selection
1) Energy allocation
2) How to measure the costs of reproduction
3) Agents of Sexual selection
4) How to measure sexual selection: Bateman gradient and other indices
5) Definition of mating success and its consequences
6) Methodological bias in the use of sexual selection indices
7) But is individual reproductive success the sole results of individual investment?
8) Fitness decomposition
9) Effect of environment on sexual selection
10) Can human induced environmental change affect sexual selection?
II Brown trout, sexual selection, and environmental variation
1) Brown trout as a biological model for sexual selection
2) Environmental change and brown trout reproduction
3) How to read this manuscript
CHAPTER II. Experimental approach and methods
I. Context
II. Experiments in semi-natural environment
1) Semi-natural conditions: the Lapitxuri spawning channel
2) Experiments timeline
3) How to recognize fish during reproduction
4) Behaviour recording
5) Reproductive success estimation
a) DNA extraction
b) Microsatellite multiplex PCR
c) Genotyping
d) Parentage analysis
6) Measures of plasma metabolites concentration in blood samples
a) Why plasma metabolites?
b) Method description
7) Differences between A, B1, and B2 experiments.
a) Experiment A: constant environment, single population.
b) Experiment B1 and B2: replication of results, population effects and environment control.
III. Natural environment: experiment C
1) Sampling sites and reproductive activity
2) Habitat variables, egg size and experimental setup
3) Survival
4) Particle size analysis
IV. A word on statistics
CHAPTER III. Sex alone: individual scale
I. Context
II. How much weight did individual invest in the reproduction? (EXP A)
III. Relationship between weight and reproductive success
IV. Metabolites as a proxy of reproductive effort
1) Initial level of metabolites
2) Metabolite variations during reproduction
V. Link between variation in weight and in metabolites
VI. Relative contribution of weight and plasma metabolites on reproductive success.
VII. Behaviours and reproductive investment
1) Digging behaviour
2) Competition between males
CHAPTER IV. Sex not alone : effect of conspecifics
I. Context
II. OSR variation
III. OSR and competition
IV. OSR, attractiveness, and phenotype availability
V. Fitness model: taking into account conspecific phenotypes in reproductive success
1) Context
2) What do we learn from raw behavioural and molecular data?
a) Bateman gradient
b) Body size as a trait of interest under selection
3) Statistical model
a) Selection indices from raw data and from the model output
b) Combined effect of male and female phenotype on the components of reproductive success
CHAPTER V. Sex in habitats: population scale
I. Context
II. Within river contrast in environment
1) Effect on offspring survival: redd scouring as the biggest environmental pressure?
2) How to explain egg size variability in Salmo trutta?
3) Does phenotype habitat matching exist in our populations?
4) What solution to face unpredictable variation?
III. Between river contrast in environment
1) Does contrast in discharge stochasticity affect OSR?
2) Does contrast in discharge affect reproductive investment?
a) Experiment A vs experiment B1
b) Experiment B1 vs experiment B2
3) Variability in reproductive effort may lead to reproductive isolation?
a) Assessment of mating success and reproductive success
b) Reproductive isolation calculation
c) Results
4) Conclusions relative to environmental stochasticity effects on reproduction in Experiments B1 and B2.
Chapter VI. Discussion
I. Remarkable results
1) Trade-off between investment and reproductive success: a new avenue
2) The benefits of handling various data sources to test a single hypothesis.
3) Take-home results for effects of environment on sexual selection
II. Effect of stochastic environment on reproductive investment and fitness
III. Limitations of the present approach
1) Other traits involved in sexual selection
2) Modeling limitation
BIBLIOGRAPHY
