Jean-François Le Galliard

How does selection operate on whole-organism functional performance capacities? A review and synthesis

Hypothesis: Natural and sexual selection should be stronger on whole-organism functional performance traits (sprinting, biting) than on correlated morphological variables. Organisms: Lizards, snakes, turtles, frogs, and fish (review of past field and laboratory studies). Field sites: Various (review of past field and laboratory studies). Methods: We reviewed existing literature on the nature and intensity of natural and sexual selection on whole-organism performance traits. We answer some key questions in regards to how selection operates on performance, and whether selection is stronger on performance compared with morphological traits. Results: We identified 23 studies that have quantified selection on performance. Natural and sexual selection were typically directional in nature, with a distinct preference for high rather than low values of performance. However, some studies uncovered no significant selection on performance, and there was also no evidence that selection was stronger on performance traits than morphological traits.

Physical performance and darwinian fitness in lizards

Strong evidence for a genetic basis of variation in physical performance has accumulated. Considering one of the basic tenets of evolutionary physiology—that physical performance and darwinian fitness are tightly linked—one may expect phenotypes with exceptional physiological capacities to be promoted by natural selection. Why then does physical performance remain considerably variable in human and other animal populations? Our analysis of locomotor performance in the common lizard (Lacerta vivipara) demonstrates that initial endurance (running time to exhaustion measured at birth) is indeed highly heritable, but natural selection in favour of this trait can be unexpectedly weak. A manipulation of dietary conditions unravels a proximate mechanism explaining this pattern. Fully fed individuals experience a marked reversal of performance within only one month after birth: juveniles with low endurance catch up, whereas individuals with high endurance lose their advantage. In contrast, dietary restriction allows highly endurant neonates to retain their locomotor superiority as they age. Thus, the expression of a genetic predisposition to high physical performance strongly depends on the environment experienced early in life.

Personality and the pace‐of‐life syndrome: variation and selection on exploration, metabolism and locomotor performances

Summary 1. Consistent individual differences in behaviour are seen in numerous animals and could be maintained by life-history trade-offs and integrated within a pace-of-life syndrome involving physiological and locomotor traits. 2. Lizard species are characterized by inter-specific variation in activity and foraging behaviours associated with differences in locomotor performances and metabolic rates. Similar syndromes could exist within species, but have not been investigated so far. 3. We scored the exploratory behaviour of newborn common lizards (Zootoca vivipara) using a neutral arena test and measured concomitantly resting metabolic rate (RMR), maximal sprint speed (MSS) and endurance capacity. Animals were released in outdoor enclosures exposed to avian predation and measured again for the same traits 1 year later. 4. Common lizards displayed consistent individual differences over a week for an exploration score associated with high activity in the neutral arena. Individual differences in three activity scores were also consistent over the first year of life. 5. Correlations among behavioural, metabolic and locomotor traits were weak, except for a marginally significant, positive correlation between exploration score and MSS and endurance at the age of 1 year. 6. Correlational survival selection was found for RMR and exploration score such that newborns with low exploration score and high RMR and newborns with high exploration score and low RMR survived better. Correlational growth selection was also found with faster growth in newborns with low exploration score and high RMR. 7. The results are discussed against recent hypotheses to explain the maintenance of animal temperaments.

CONFLICT OVER MULTIPLE‐PARTNER MATING BETWEEN MALES AND FEMALES OF THE POLYGYNANDROUS COMMON LIZARDS

Abstract The optimal number of mate partners for females rarely coincides with that for males, leading to a potential sexual conflict over multiple‐partner mating. This suggests that the population sex ratio may affect multiple‐partner mating and thus multiple paternity. We investigate the relationship between multiple paternity and the population sex ratio in the polygynandrous common lizard (Lacerta vivipara). In six populations the adult sex ratio was biased toward males, and in another six populations the adult sex ratio was biased toward females, the latter corresponding to the average adult sex ratio encountered in natural populations. In males the frequency and the degree of polygyny were lower in male‐biased populations, as expected if competition among males determines polygyny. In females the frequency of polyandry was not different between treatments, and polyandrous females produced larger clutches, suggesting that polyandry might be adaptive. However, in male‐biased populations females suffered from reduced reproductive success compared to female‐biased populations, and the number of mate partners increased with female body size in polyandrous females. Polyandrous females of male‐biased populations showed disproportionately more mating scars, indicating that polyandrous females of male‐biased populations had more interactions with males and suggesting that the degree of multiple paternity is controlled by male sexual harassment. Our results thus imply that polyandry may be hierarchically controlled, with females controlling when to mate with multiple partners and male sexual harassment being a proximate determinant of the degree of multiple paternity. The results are also consistent with a sexual conflict in which male behaviors are harmful to females.

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara. This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.

Patterns and processes of dispersal behaviour in arvicoline rodents

A good understanding of mammalian societies requires measuring patterns and comprehending processes of dispersal in each sex. We investigated dispersal behaviour in arvicoline rodents, a subfamily of mammals widespread in northern temperate environments and characterized by a multivoltine life cycle. In arvicoline rodents, variation in life history strategies occurs along a continuum from precocial to delayed maturation that reflects seasonal and ecological fluctuations. We compared dispersal across and within species focusing on the effects of external (condition‐dependent) and internal (phenotype‐dependent) factors. Our data revealed substantial, unexplained variation between species for dispersal distances and a strong variation within species for both dispersal distance and fraction. Some methodological aspects explained variation across studies, which cautions against comparisons that do not control for them. Overall, the species under consideration display frequent short‐distance dispersal events and extremely flexible dispersal strategies, but they also have hitherto unexpected capacity to disperse long distances. Female arvicolines are predominantly philopatric relative to males, but we found no clear association between the mating system and the degree of sex bias in dispersal across species. Dispersal is a response to both various proximate and ultimate factors, including competition, inbreeding avoidance, mate searching and habitat quality. In particular, our review suggests that costs and benefits experienced during transience and settlement are prime determinants of condition dependence. Patterns of phenotype‐dependent dispersal are idiosyncratic, except for a widespread association between an exploration/activity syndrome and natal dispersal. Consequences for population dynamics and genetic structures are discussed.

Inconsistency between Different Measures of Sexual Selection

Measuring the intensity of sexual selection is of fundamental importance to the study of sexual dimorphism, population dynamics, and speciation. Several indices, pools of individuals, and fitness proxies are used in the literature, yet their relative performances are strongly debated. Using 12 independent common lizard populations, we manipulated the adult sex ratio, a potentially important determinant of the intensity of sexual selection at a particular time and place. We investigated differences in the intensity of sexual selection, as estimated using three standard indices of sexual selection—the standardized selection gradient (β′), the opportunity of selection (I), and the Bateman gradient (βss)—calculated for different pools of individuals and different fitness proxies. We show that results based on estimates of I were the opposite of those derived from the other indices, whereas results based on estimates of β′ were consistent with predictions derived from knowledge about the species’ mating system. In addition, our estimates of the strength and direction of sexual selection depended on both the fitness proxy used and the pool of individuals included in the analysis. These observations demonstrate inconsistencies in distinct measures of sexual selection and underscore the need for caution when comparing studies and species.

Networking our way to better ecosystem service provision

The ecosystem services (EcoS) concept is being used increasingly to attach values to natural systems and the multiple benefits they provide to human societies. Ecosystem processes or functions only become EcoS if they are shown to have social and/or economic value. This should assure an explicit connection between the natural and social sciences, but EcoS approaches have been criticized for retaining little natural science. Preserving the natural, ecological science context within EcoS research is challenging because the multiple disciplines involved have very different traditions and vocabularies (common-language challenge) and span many organizational levels and temporal and spatial scales (scale challenge) that define the relevant interacting entities (interaction challenge). We propose a network-based approach to transcend these discipline challenges and place the natural science context at the heart of EcoS research.

Effects of individual condition and habitat quality on natal dispersal behaviour in a small rodent

1. Individuals should benefit from settling in high-quality habitats, but dispersers born under favourable conditions have a better physical condition and should therefore be more successful at settling in high-quality habitats. 2. We tested these predictions with root voles (Microtus oeconomus) by a manipulation of individual condition through litter-size enlargement and reduction during lactation combined with a manipulation of habitat quality through degradation of the vegetation cover. We accurately monitored movements of 149 juveniles during a settlement and breeding period of 3 months. 3. The litter size treatment had long-lasting effects on body size, life-history traits and home range size, but did not influence dispersal behaviour. 4. Different stages of dispersal were influenced by habitat quality. In low-quality patches, females dispersed earlier, spent more time prospecting their environment before settling, and settlers had a smaller adult body size than in high-quality patches. Preference and competition for high-quality patches is likely adaptive as it increased fitness both in terms of survival and reproduction. 5. We found no interactive effect of individual condition and habitat quality on natal dispersal and habitat selection. 6. These findings suggest that immediate conditions are more important determinants of dispersal decisions than conditions experienced early in life.

Territory ownership and familiarity status affect how much male root voles (Microtus oeconomus) invest in territory defence

Neighbour–stranger discrimination occurs when individuals respond with more aggression to strangers than to territorial neighbours—a phenomenon termed the “dear enemy phenomenon” (DEP). We investigated the DEP with male and female root voles (Microtus oeconomus Pallas 1776) using field dyadic arena tests conducted in enclosures where we could test for the effects of familiarity (familiar versus stranger), ownership (resident versus intruder status) and resource-holding potential (body mass) on territorial behaviours. The results showed that males put more effort into territorial defence than females, and males could discriminate between neighbours and strangers. In males, aggressiveness was influenced by a significant two-way interaction between treatment and ownership. Male residents were more aggressive towards stranger intruders than towards neighbour intruders, while male intruders were less aggressive towards stranger residents than towards neighbour residents. In females, neither treatment nor ownership status had a significant effect on aggressiveness. Familiar males performed more social behaviours but less non-social behaviours than stranger males. Furthermore, there was a clear dominance hierarchy between residents and intruders in stranger dyads, with the male territory holders dominating the intruder in pairwise interactions. To our knowledge, these results demonstrate for the first time DEP in a small mammal with a known pedigree and present the first evidence for “prior resident advantage” in voles. We argue that both ownership status and familiarity status affect how much an individual invests in territory defence. The benefits of neighbour–stranger discrimination for male root voles and the absence of neighbour–stranger discrimination in female root voles are discussed.