Marie-Claude Bel-Venner

Unexpected male choosiness for mates in a spider

Sexual selection theory traditionally considers choosiness for mates to be negatively related to intra-sexual competition. Males were classically considered to be the competing, but not the choosy, sex. However, evidence of male choosiness is now accumulating. Male choosiness is expected to increase with an individuals competitive ability, and to decrease as intra-sexual competition increases. However, such predictions have never been tested in field conditions. Here, we explore male mate choice in a spider by studying size-assortative pairing in two natural sites that strongly differ in the level of male–male competition. Unexpectedly, our results demonstrate that mate choice shifts from opportunism to high selectivity as competition between males increases. Males experiencing weak competition did not exhibit size-related mating preferences. By contrast, when competition was intense we found strong size-assortative pairing due to male choice: while larger, more competitive males preferentially paired with larger, more fecund females, smaller males chose smaller females. Thus, we show that mating preferences of males vary with their competitive ability. The distinct preferences exhibited by males of different sizes seem to be an adaptive response to the lower reproductive opportunities arising from increased competition between males.

A handbook for uncovering the complete energetic budget in insects: the van Handel's method (1985) revisited

Insects comprise relevant biological models for investigating nutrient acquisition and allocation processes in the context of life‐history ecology and evolution. However, empirical investigations are still partly limited by the lack of availability of simple methods for simultaneously estimating the four major energetic components (i.e. lipids, free sugars, glycogen and proteins) in the same individual. In the present work, we validate a fast, reproducible and cheap method for overcoming this problem that uses different solvents successively. First, proteins are solubilized in a phosphate‐lysis buffer and then quantified according to the classical Bradford assay procedure. In a second step, a chloroform–methanol mixture is added to the aqueous phase, which allows assay of the total lipid fraction, as well as the free sugars and glycogen in the same insect homogenate. In addition, a micro‐separation procedure is adapted to partition the total lipids into neutral (mainly stored lipids) and polar (mainly structural lipids) components. Although these assays are conducted sequentially in the same individual, the sensitivity of our method remains high: the estimated amount of each energetic compartment does not differ from that obtained with former, partial methods. Our method should thus largely improve our knowledge about nutrient acquisition and allocation among insects not only in laboratory‐reared individuals, but also in animals caught in the wild. Descriptions and recommendations are given at each step of the protocol to adapt the procedure to various insect species. Finally, to prevent misinterpretation of data generated in accordance with this protocol, the limits of our method are discussed in the light of life‐history studies.

Coexistence of Insect Species competing for a pulsed resource: toward a unified theory of biodiversity in fluctuating environments

Background One major challenge in understanding how biodiversity is organized is finding out whether communities of competing species are shaped exclusively by species-level differences in ecological traits (niche theory), exclusively by random processes (neutral theory of biodiversity), or by both processes simultaneously. Communities of species competing for a pulsed resource are a suitable system for testing these theories: due to marked fluctuations in resource availability, the theories yield very different predictions about the timing of resource use and the synchronization of the population dynamics between the competing species. Accordingly, we explored mechanisms that might promote the local coexistence of phytophagous insects (four sister species of the genus Curculio) competing for oak acorns, a pulsed resource. Methodology/Principal Findings We analyzed the time partitioning of the exploitation of oak acorns by the four weevil species in two independent communities, and we assessed the level of synchronization in their population dynamics. In accordance with the niche theory, overall these species exhibited marked time partitioning of resource use, both within a given year and between different years owing to different dormancy strategies between species, as well as distinct demographic patterns. Two of the four weevil species, however, consistently exploited the resource during the same period of the year, exhibited a similar dormancy pattern, and did not show any significant difference in their population dynamics. Conclusions/Significance The marked time partitioning of the resource use appears as a keystone of the coexistence of these competing insect species, except for two of them which are demographically nearly equivalent. Communities of consumers of pulsed resources thus seem to offer a promising avenue for developing a unifying theory of biodiversity in fluctuating environments which might predict the co-occurrence, within the same community, of species that are ecologically either very similar, or very different.

Make Love Not War: When Should Less Competitive Males Choose Low-Quality but Defendable Females?

Male choosiness for mates is an underexplored mechanism of sexual selection. A few theoretical studies suggest that males may exhibit—but only under rare circumstances—a reversed male mate choice (RMMC; i.e., highly competitive males focus on the most fecund females, while the low‐quality males exclusively pair with less fecund mates to avoid being outcompeted by stronger rivals). Here we propose a new model to explore RMMC by relaxing some of the restrictive assumptions of the previous models and by considering an extended range of factors known to alter the strength of sexual selection (males’ investment in reproduction, difference of quality between females, operational sex ratio). Unexpectedly, we found that males exhibited a reversed mate choice under a wide range of circumstances. RMMC mostly occurs when the female encounter rate is high and males devote much of their time to breeding. This condition‐dependent strategy occurs even if there is no risk of injury during the male‐male contest or when the difference in quality between females is small. RMMC should thus be a widespread yet underestimated component of sexual selection and should largely contribute to the assortative pairing patterns observed in numerous taxa.

Body-mass-dependent cost of web-building behavior in an orb weaving spider, Zygiella x-notata.

In numerous spider species, reproductive success of adult females has been shown to be positively correlated with their body mass. We suggest, however, that spiders may incur greater foraging costs as their body mass increases due to the numerous and complex locomotor bouts needed to build an orb-web. Such a body-mass-dependent cost should, in turn, affect the web-building decisions of spiders. In the laboratory, we tested the influence of body mass on energetic expenditure (measured as mass loss) during web-building behavior in Zygiella x-notata. Our results showed (1) that energetic costs associated with web-building were closely related to body mass and to web-building activity, and (2) that as their body mass increased, spiders reduced the amount of silk used per web, while their foraging effort simultaneously increased. This work gives new insights into web-building behavior and energy allocation strategies of weaving spiders.

Endosymbiont diversity among sibling weevil species competing for the same resource

BackgroundWhereas the impact of endosymbionts on the ecology of their hosts is well known in some insect species, the question of whether host communities are influenced by endosymbionts remains largely unanswered. Notably, the coexistence of host species competing with each other, which is expected to be stabilized by their ecological differences, could be facilitated by differences in their endosymbionts. Yet, the composition of endosymbiotic communities housed by natural communities of competing host species is still almost unknown. In this study, we started filling this gap by describing and comparing the bacterial endosymbiotic communities of four sibling weevil species (Curculio spp.) that compete with each other to lay eggs into oak acorns (Quercus spp.) and exhibit marked ecological differences.ResultsAll four species housed the primary endosymbiont Candidatus Curculioniphilus buchneri, yet each of these had a clearly distinct community of secondary endosymbionts, including Rickettsia, Spiroplasma, and two Wolbachia strains. Notably, three weevil species harbored their own predominant facultative endosymbiont and possessed the remaining symbionts at a residual infection level.ConclusionsThe four competing species clearly harbor distinct endosymbiotic communities. We discuss how such endosymbiotic communities could spread and keep distinct in the four insect species, and how these symbionts might affect the organization and species richness of host communities.

Ecophysiological attributes of adult overwintering in insects: insights from a field study of the nut weevil, Curculio nucum

Abstract Diapausing insect species have evolved a great diversity of life cycles, although overwintering occurs at a single development stage within most species. Understanding why diapause has evolved towards a given life stage requires investigation of both the ecological and physiological attributes. Notably, it is suggested that adult overwintering is more energy‐demanding than larval overwintering but it brings fitness gains by allowing adults to be synchronized with their seasonal requisites through an early spring emergence. This hypothesis is tested in field conditions in the nut weevil Curculio nucum, whose life cycle comprises an obligate 2‐year, nonfeeding underground phase, including a larval, followed by an adult, overwintering. In this species, adult wintering leads to an early spring emergence; at first glance, however, this does not enhance synchronization between weevils and their host because adults emerge more than 1 month before starting to breed. It is suggested that adult overwintering ultimately evolved in response to the phenology of the host, by allowing females to oviposit in nuts before their full sclerotinization. Adult overwintering appears to be costly because adults postpone reproduction for 1 year, incur a significant weight loss and require feeding before egg laying. Surprisingly, lipids are unaffected during diapause, lipogenesis even being likely in the summer metamorphosis. These results suggest that the lipids involved in egg production may entirely come from the larval stages, whereas the other nutrients are acquired through adult feeding but this remains to be tested.

Fruiting Strategies of Perennial Plants: A Resource Budget Model to Couple Mast Seeding to Pollination Efficiency and Resource Allocation Strategies

Masting, a breeding strategy common in perennial plants, is defined by seed production that is highly variable over years and synchronized at the population level. Resource budget models (RBMs) proposed that masting relies on two processes: (i) the depletion of plant reserves following high fruiting levels, which leads to marked temporal fluctuations in fruiting; and (ii) outcross pollination that synchronizes seed crops among neighboring trees. We revisited the RBM approach to examine the extent to which masting could be impacted by the degree of pollination efficiency, by taking into account various logistic relationships between pollination success and pollen availability. To link masting to other reproductive traits, we split the reserve depletion coefficient into three biological parameters related to resource allocation strategies for flowering and fruiting. While outcross pollination is considered to be the key mechanism that synchronizes fruiting in RBMs, our model counterintuitively showed that intense masting should arise under low-efficiency pollination. When pollination is very efficient, medium-level masting may occur, provided that the costs of female flowering (relative to pollen production) and of fruiting (maximum fruit set and fruit size) are both very high. Our work highlights the powerful framework of RBMs, which include explicit biological parameters, to link fruiting dynamics to various reproductive traits and to provide new insights into the reproductive strategies of perennial plants.

From Income to Capital Breeding: When Diversified Strategies Sustain Species Coexistence

There is empirical evidence of many diversified ways for energy to be acquired and allocated to reproduction, notably with strategies ranging from strict income breeding (females fueling their gametes with energy gained concomitantly during reproduction) to strict capital breeding (females storing nutrients prior reproduction). Until now, the question of whether diversification of these strategies might impact the way communities are organized has not been considered. Here, we suggest that diversified resource allocation strategies among competing species may contribute to their coexistence. We examined this hypothesis by focusing on communities composed of four phytophagous insect species that coexist and compete for egg-laying sites. From wild-caught females, we determined precisely the breeding period of each species and we described their resource acquisition and allocation to reproduction dynamics. We quantified in each species the total amount of larval energy stored by newly-emerging females and then monitored the total energy budget of females caught in the field before and throughout their breeding period. We found that the four sibling weevil species are markedly segregated along the income-capital-breeding continuum, which is correlated with clear time partitioning in their laying activity. Our results suggest that diversified resource allocation strategies might contribute to time partitioning of plant resources exploitation and thus indirectly to their coexistence. This work should further encourage studies examining the extent to which competitive coexistence might be affected by diversification of income-capital breeding strategies together with the intensity of interspecific competition, and considering the divergent evolution of these strategies.

Revisiting the link between breeding effort and oxidative balance through field evaluation of two sympatric sibling insect species

The idea that oxidative stress could be a major force governing evolutionary trade‐offs has recently been challenged by experimental approaches in laboratory conditions, triggering extensive debates centered on theoretical and methodological issues. Here, we revisited the link between oxidative stress and reproduction by measuring multiple antioxidant and oxidative damages in wild‐caught females of two sibling weevil species (Curculio elephas, C. glandium). The strength of our study arised from (1) studied species that were sympatric and exploited similar resource, but displayed contrasting reproductive strategies and (2) individuals were sampled throughout adult life so as to relate oxidative status to breeding effort. We found that the short‐lived C. elephas sacrifices red‐ox homeostasis for immediate reproduction upon emergence as characterized by low antioxidant defenses and elevated oxidative damage. Comparatively, C. glandium massively invests in antioxidant and maintains low oxidative damage, which may contribute to their extended prereproductive period. Intriguingly, we also reveal, for the first time in a field study, an unexpected reactivation of antioxidant defenses with the onset of reproduction. Our results thus support the existence of a strong, but complex relationship between oxidative stress and life‐history evolution and highlight the need for a finer‐scale picture of antioxidant strategies.