Marie-Jeanne Holveck

Long-term effects of manipulated natal brood size on metabolic rate in zebra finches

Long-term effects of developmental conditions on health, longevity and other fitness components in humans are drawing increasing attention. In evolutionary ecology, such effects are of similar importance because of their role in the trade-off between quantity and quality of offspring. The central role of energy consumption is well documented for some long-term health effects in humans (e.g. obesity), but little is known of the long-term effects of rearing conditions on energy requirements later in life. We manipulated the rearing conditions in zebra finches (Taeniopygia guttata) using brood size manipulation and cross-fostering. It has previously been shown in this species that being reared in a large brood has negative fitness consequences, and that such effects are stronger in daughters than in sons. We show that, independent of mass, standard metabolic rate of 1-year-old birds was higher when they had been reared in a large brood, and this is to our knowledge the first demonstration of such an effect. Furthermore, the brood size effect was stronger in daughters than in sons. This suggests that metabolic efficiency may play a role in mediating the long-term fitness consequences of rearing conditions.

Sex-biased predation by polecats influences the mating system of frogs

In agile frogs, Rana dalmatina, an increase in male–biased operational sex ratio and in male abundance results in the emergence of alternative male mating behaviour in the form of searching. As a consequence, females are coerced into mating with multiple males, which in turn increases the level of conflict between the sexes. Selective predation on males by the European polecat, Mustela putorius, decreases the occurrence of polyandry. In ponds visited by polecats, the sex ratio is less male biased than in ponds where polecats are absent. As a result most males call to attract females and fewer males actively search for females. Females are able to choose between calling males and mate with a single male. Thus, predation by polecats is found to influence sex ratio, male abundance and sexual conflict in a frog mating system, restricting the opportunity for multiple mating.

Can eggs in a cavity be a female secondary sexual signal? Male nest visits and modelling of egg visual discrimination in blue tits

Eggshell colouration is thought to function as a female-specific secondary sexual trait. While tests of this idea are rapidly accumulating in cavity-nesting birds, some fundamental underlying assumptions remain rarely investigated: namely, can males see eggshell coloration and perceive colour differences between the eggs of different females? We tested these two key assumptions in a natural population of blue tits (Cyanistes caeruleus). Using transponders, we tracked male nest visits and found that all males visited their nest-boxes while eggs were present and often visually accessible. Interestingly, some males also visited neighbouring nests. We then tested whether birds could detect eggshell coloration using models of avian colour vision; models were performed with and without limitations on visual performance owing to dim light. Both models found that differences in eggshell brightness were often easier to discriminate than differences in colour; there was more contrast in white eggshell background between clutches than within and its contrast against nest background was repeatable within clutches, suggesting these features could act as signals. Yet, the detectability of these contrasts depended entirely on model assumptions of visual limitations. Consequently, we need a better understanding of underlying visual mechanisms in dim-light environments and behavioural discrimination experiments before confirming the signalling potential of eggshell coloration.

Are high-quality mates always attractive? State-dependent mate preferences in birds and humans

Sexual selection theory posits that females should choose mates in a way that maximises their reproductive success. But what exactly is the optimal choice? Most empirical research is based on the assumption that females seek a male of the highest possible quality (in terms of the genes or resources he can provide), and hence show directional preferences for indicators of male quality. This implies that attractiveness and quality should be highly correlated. However, females frequently differ in what they find attractive. New theoretical and empirical insights provide mounting evidence that a females own quality biases her judgement of male attractiveness, such that male quality and attractiveness do not always coincide. A recent experiment in songbirds demonstrated for the first time that manipulation of female condition can lead to divergent female preferences, with low-quality females actively preferring low-quality males over high-quality males. This result is in line with theory on state-dependent mate choice and is reminiscent of assortative mating preferences in humans. Here we discuss the implications of this work for the study of mate preferences.

Eggshell spottiness reflects maternally transferred antibodies in blue tits.

Blue-green and brown-spotted eggshells in birds have been proposed as sexual signals of female physiological condition and egg quality, reflecting maternal investment in the egg. Testing this hypothesis requires linking eggshell coloration to egg content, which is lacking for brown protoporphyrin-based pigmentation. As protoporphyrins can induce oxidative stress, and a large amount in eggshells should indicate either high female and egg quality if it reflects the females high oxidative tolerance, or conversely poor quality if it reflects female physiological stress. Different studies supported either predictions but are difficult to compare given the methodological differences in eggshell-spottiness measurements. Using the blue tit Cyanistes caeruleus as a model species, we aimed at disentangling both predictions in testing if brown-spotted eggshell could reflect the quality of maternal investment in antibodies and carotenoids in the egg, and at improving between-study comparisons in correlating several common measurements of eggshell coloration (spectral and digital measures, spotted surface, pigmentation indices). We found that these color variables were weakly correlated highlighting the need for comparable quantitative measurements between studies and for multivariate regressions incorporating several eggshell-color characteristics. When evaluating the potential signaling function of brown-spotted eggshells, we thus searched for the brown eggshell-color variables that best predicted the maternal transfer of antibodies and carotenoids to egg yolks. We also tested the effects of several parental traits and breeding parameters potentially affecting this transfer. While eggshell coloration did not relate to yolk carotenoids, the eggs with larger and less evenly-distributed spots had higher antibody concentrations, suggesting that both the quantity and distribution of brown pigments reflected the transfer of maternal immune compounds in egg yolks. As yolk antibody concentrations were also positively related to key proxies of maternal quality (egg volume, number, yellow feather brightness, tarsus length), eggshells with larger spots concentrated at their broad pole may indicate higher-quality eggs.

The composition of cuticular compounds indicates body parts, sex and age in the model butterfly Bicyclus anynana (Lepidoptera)

Chemical communication in insects’ sexual interactions is well-known to involve olfaction of volatile compounds called sex pheromones. In theory, sexual chemical communication may also involve chemicals with low or no volatility exchanged during precopulatory gustatory contacts. Yet, knowledge on this latter type of chemicals is so far mostly restricted to the Drosophila fly model. Here we provide the most comprehensive characterization to date of the cuticular chemical profile, including both volatile and non-volatile compounds, of a model butterfly, Bicyclus anynana. First, we characterized the body distribution of 103 cuticular lipids, mostly alkanes and methyl-branched alkanes, by gas chromatography coupled to mass spectrometry (GC-MS). Second, we developed a multivariate statistical approach to cope with such complex chemical profiles and showed that variation in the presence or abundance of a subset of the cuticular lipids indicated body parts, and traits involved in B. anynana mate choice, namely sex and age. Third, we identified the chemical structure of the 20 most indicative compounds, which were on average more abundant (1346.4 ± 1994.6 ng; mean ± SD) than other, likely less indicative, compounds (225.9 ± 507.2 ng; mean ± SD). Fourth, we showed that wings and legs displayed most of the chemical information found on the entire body of the butterflies. Fifth, we showed that non-random gustatory contacts occurred between specific male and female body parts during courtship. The body parts mostly touched by the conspecific displayed the largest between-sex differentiation in cuticular composition. Altogether, the large diversity of cuticular lipids in B. anynana, which exceeds the one of Drosophila flies, and its non-random distribution and evaluation across individuals, together suggest that gustatory information is likely exchanged during sexual interactions in Lepidoptera.

Dense, small and male-biased cages exacerbate male–male competition and reduce female choosiness in Bicyclus anynana

Sexual selection is increasingly recognized to depend upon, and to fluctuate with, major ecological factors in natural environments. The operational sex ratio (OSR) and population density can affect the opportunity for, and strength of, sexual selection but their effects are rarely taken into account in laboratory behavioural studies. In Bicyclus anynana, a model butterfly for mate choice studies, the experimental set-up widely used in laboratories often involves very high densities compared to the field, malebiased sex ratios and small cage volumes. We hypothesized that these conditions impede the proper expression of female mating preference by promoting male competition and sexual harassment of females. Using various cage volumes, we separately manipulated OSR and density to cover the range of values used in B. anynana laboratory mating experiments and to approach field values. Male competition, quantified by the number and duration of courtships aborted by males, became stronger with increasing densities, specifically under more male-biased sex ratios, and decreasing cage volumes. Thus, male eagerness to mate was essentially due to the use of small cage volumes and very high experimental densities. Concomitantly, female choosiness, quantified by the proportion of rejections of male mating attempts, decreased with increasing densities under a male-biased sex ratio. Females also accepted more matings with decreasing cage volume, and mated more rapidly with increasing density. We conclude that the laboratory social environments frequently used to test mate choice in B. anynana, with unnaturally high densities and male-biased sex ratios, exacerbate maleemale competition and strongly hinder female choice, biasing the estimates of the strength and direction of sexual selection that were shaped under very different natural environments in the wild. We propose a set-up for B. anynana mate choice studies that allows the assessment of female choosiness in statistically robust mating experiments.

Laboratory social environment biases mating outcome: a first quantitative synthesis in a butterfly

Sexual selection is by essence social selection: an individual’s fitness is partly determined by the phenotype of its social partners (i.e., the social environment). Nevertheless, most behavioral studies on mating patterns and sexual selection are conducted in laboratory standardized conditions, and it is unclear how potential laboratory-induced social biases affect mating outcome. The social environment may actually dictate which of female mate choice or male-male competition is the primary determinant of mating outcome. This matters because we expect sexually selected traits to evolve differently if mating outcome is determined by female mate choice or by male-male competition. We address this issue by performing an in-depth quantitative synthesis testing the effects of common extrinsic (population density, sex ratio), intrinsic (age), and laboratory-induced (cage volume, experimental duration) biases of the social environment of adults on mating outcome. For this, we used the butterfly Bicyclus anynana, as it provides a reasonable sampling of mating experiments in diverse laboratory conditions (i.e., 31 publications from 7 different laboratories since 2001). We found that all tested social environmental variables displayed strong variation across B. anynana mating studies, and that most variables had significant effects usually in interaction with another variable and with opposite effects between sexes. Hence, mating outcome is affected by laboratory biases on the social environment. Our quantitative synthesis offers a first case example of the effects of a pervasive and recurrent issue in animal behavioral research on sexual selection, i.e., the need to root mating experiments in ecologically relevant laboratory environments, in order to produce meaningful results about the selective force(s) driving the evolution of sexually selected traits in nature.Significance statementMating outcome is biased by the laboratory social environment in which experiments are conducted. Male and female age, density, ratio, as well as cage volume and experimental duration all affect mating proportions, and this blurs our understanding of how sexual selection shapes sexually selected traits in the wild. This first systematic review was conducted on 31 studies in a single butterfly species, but our results are likely relevant in any taxonomic group.

Commentary on Kehl et al. “Young male mating success is associated with sperm number but not with male sex pheromone titres”

Over the last years, several studies suggested that male courtship activity is more important than female preference for male secondary sexual traits in determining male mating success in the butterfly Bicyclus anynana. We use Kehl et al. (Front Zool 12, 2015)s study and related publications, to highlight three methodological and conceptual aspects of laboratory experiments that distort the social environment compared to natural conditions. We argue that such experimental biases prevent the expression of female mate choice and artificially inflate the role of male activity in determining mating success. We really want to stress that any work performed in laboratory conditions using extreme cage densities or sizes impedes female mate choice and promotes male-male competition when sexual conflict occurs about mating decisions. Hence, such studies, and the derived conclusions, are only applicable to ecologically-irrelevant conditions and cannot be extrapolated to more natural laboratory or field conditions. Our concerns may be relevant to many behavioural studies quantifying sexual selection across taxa. This commentary adds to the increasing scientific awareness that: i) mating outcome is, across taxa, the result of a sexual conflict whose outcome is under female, and not male, control; ii) the social environment used to quantify mating success is of utmost importance to produce reliable estimates of the strength and the direction of sexual selection on sexually-selected traits, as they evolve in nature.

Timing of Breeding in an Ecologically Trapped Bird

In human-modified environments, organisms may prefer to use habitats where their reproductive performance is lower compared to alternative options. Many such ecological traps occur in seasonally changing environments. Although the timing of breeding has been shown to impact reproductive performance in a variety of organisms, it has never been considered as a potential mechanism underlying ecological traps. We address this issue with a migratory bird, the red-backed shrike, breeding in a human-modified, farmland-forest landscape. Shrikes prefer breeding in forest clear-cuts where their reproductive performance is lower than in less attractive farmland. We compared brood size and quality of early (first broods) and delayed breeders (replacement broods) between the two habitats. We found a stronger seasonal decrease in reproductive performance in preferred forest clear-cuts than in farmland. Food resources were slightly more abundant in forest than in farmland at the beginning of the season but depleted more steeply in forest by the end of the breeding season. By contrast, the phenotypic quality of breeders did not decline over the course of the season in either habitat. This is the first report that the timing of breeding relative to the seasonal change in key resources may play a significant role in explaining low reproductive performance in ecological traps.