Multiple cues are often used for mate choice in complex environments, potentially entailing mismatches in the information conveyed by different sources. We address the consequences of this ...information mismatch for receivers using the spider mite Tetranychus urticae, in which virgin females are highly valuable mates compared to mated females, given first male sperm precedence. Accordingly, males are known to prefer virgins and distinguish them using cues from the females themselves and that they leave on the substrate. Whereas cues from females are highly reliable, those left on the substrate may not reflect the real female mating status if females move and/or mate. Here, we tested the consequences of such mismatch by exposing males to mated or virgin females on patches previously impregnated with cues deposited by females of either mating status. Male mating attempts were solely affected by substrate cues while female acceptance and the number of mating events were independently affected by both cues. Copulation duration, in contrast, depended mainly on the mating status of the female, with the number of copulations and the total time spent mating being intermediate in environments with mismatched information. We also show that males incur mating costs, reflected in reduced survival in environments with virgin cues. These results suggest that substrate cues left by females are instrumental for males to find their mates. However, in environments with mismatched information, males may pay survival costs without the associated benefit of mating with virgins, or they may lose opportunities to mate with virgins by responding to substrate cues from mated females. The benefit of using multiple cues will then hinge upon the frequency of information mismatch, which itself should vary with the dynamics of populations.
Mismatches between cues can occur when they persist in the environment for different periods of time, potentially increasing uncertainty about which mate to choose. We found that patches with a mismatch between cues signalling female mating status led to intermediate survival costs in males, with the substrate cues left by females being instrumental for males to find their mates quicker but at the expense of mating with females and not fertilising their offspring.
Reproduction is generally more sensitive to high temperatures than survival and arguably a better predictor of the response of populations to climate change than survival estimates. Still, how ...temperature simultaneously impacts male and female reproductive success, the mating system and the operational sex ratio remains an open question.
Here, we addressed how a sublethal high temperature affects the reproductive system of the haplodiploid spider mite Tetranychus urticae. Males and females maintained at 25 or 36°C during development were paired and the fertility of both sexes, their mating and remating eagerness, and the paternity of the offspring of females with different mating histories were measured.
Female and male fertility decreased at 36°C compared to 25°C, resulting in lower offspring production and a more male‐biased sex ratio, respectively, because of haplodiploidy. However, when either heat‐stressed females or females that mated with heat‐stressed males remated, there was a shift in paternity share, with more than one male contributing to the offspring. This was accompanied by reduced mating eagerness in pairs with partially sterile males and increased remating eagerness in pairs in which at least one sex was partially sterile in the first mating.
The observed temperature‐induced changes in female remating eagerness and sperm use allowed restoring the offspring sex ratio, by increasing the proportion of fertilized offspring, but did not lead to the recovery of offspring number.
The temperature‐induced changes in the mating behaviour and mating system should alter the interactions within and between the sexes, and with it the strength of sexual selection and sexual conflict in this species. Whether such changes are sufficient to prevent population extinction, despite the inability to recover offspring number, remains an open question.
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Read the free Plain Language Summary for this article on the Journal blog.
Agricultural fields are typically simplified ecosystems compared to natural sites, a characteristic that has long‐attracted researchers in Ecology and Evolution. In recent years, there has been a ...rising interest in understanding how agricultural systems are shaped by evolution in the context of changing agricultural practices by integrating biological information of crop systems. This editorial introduces the special issue “Evolution in agricultural systems,” incorporating the articles published within this issue into three general areas of research: phenotypic and genetic responses to the environment, biotic interactions and the role of microbes. Together, this body of work unveils unforeseen complexity at all levels, from microbes to trophic chains. Understanding such complexity is critical not only to better understand natural systems, but also if we wish to improve the sustainability of the food system.
Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these ...traits in sub‐divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta‐populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) or global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female‐biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In contrast, the scale of competition did not strongly affect sex allocation. Offspring sex ratio and female fecundity were unaffected by the number of mates, but female fecundity was highest when their mates evolved under budding dispersal, suggesting these males inflict less harm than those evolving under random dispersal. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. Moreover, selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.
We used experimental evolution to investigate how the scale of competition (Local or Global) and type of dispersal (Budding or Random) impacts sex allocation and sexual conflict in the spider mite, Tetranychus urticae. After ca. 30 generations of selection, populations evolving under budding dispersal showed lower levels of sexual conflict and produced less female‐biased offspring sex ratios.
One of the fundamental aims of ecological, epidemiological and evolutionary studies of host–parasite interactions is to unravel which factors affect parasite virulence. Theory predicts that virulence ...and transmission are correlated by a trade-off, as too much virulence is expected to hamper transmission owing to excessive host damage. Coinfections may affect each of these traits and/or their correlation. Here, we used inbred lines of the spider mite Tetranychus urticae to test how coinfection with T. evansi impacted virulence–transmission relationships at different conspecific densities. The presence of T. evansi on a shared host did not change the relationship between virulence (leaf damage) and the number of transmitting stages (i.e. adult daughters). The relationship between these traits was hump-shaped across densities, both in single and coinfections, which corresponds to a trade-off. Moreover, transmission to adjacent hosts increased in coinfection, but only at low T. urticae densities. Finally, we tested whether virulence and the number of daughters were correlated with measures of transmission to adjacent hosts, in single and coinfections at different conspecific densities. Traits were mostly independent, meaning that interspecific competitors may increase transmission without affecting virulence. Thus, coinfections may impact epidemiology and parasite trait evolution, but not necessarily the virulence–transmission trade-off. This article is part of the theme issue ‘Diversity-dependence of dispersal: interspecific interactions determine spatial dynamics’.
The UN Decade on Ecosystem Restoration is focussing attention and resources on restoration globally. Nowhere is this more crucial than in tropical forests that harbor immense biodiversity, but have ...also undergone widespread deforestation over the past few decades. We performed a meta-analysis to investigate how biodiversity features respond to forest restoration across the Brazilian Atlantic Forest (BAF), one of the most threatened biodiversity hotspots in the world. We assembled biodiversity in different metrics of structure and diversity features of three taxonomic groups (vascular plants, soil microorganisms, and invertebrates), generating a dataset with 2370 observations from 76 primary studies. We quantified the incomplete recovery of biodiversity (i.e., the rate of recovery to a pre-disturbance state) occurring during the restoration process, which we called the ‘recovery gap’. Our results revealed that forests undergoing restoration in the BAF show a recovery gap of 34% for structure features and 22% for diversity features in comparison to reference reforests, considering all taxonomic groups investigated. For vascular plants, soil microorganisms, and invertebrates the recovery gap ranged between 46 and 47%, 16–26%, and 4–7%, respectively. Overall, the recovery gap was influenced by the interaction of restoration actions (i.e., the past land use, restoration age and restoration approach – active and passive restoration), however, structure features responded more sensitively to the time elapsed since restoration started, while the recovery gap for diversity features depended more on the past land-use. Our study can help guide the prioritization of the aforenamed taxonomic groups in restoration, the regulation of potential biodiversity offsetting policies in the BAF, and understanding how coupled biodiversity features respond to the interaction of environmental conditions and restoration actions in a high fragmented tropical landscape.
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•Diversity features showed a smaller recovery gap in the BAF.•The recovery gap for structure features shortened after 20 years of restoration.•Recovery depended more on the taxonomic group than the biodiversity feature.•The recovery gap was higher for vascular plants than the other taxonomic groups.
The damage that herbivores inflict on plants is a key component of their interaction. Several methods have been proposed to quantify the damage caused by chewing insects, but such methods are not ...very successful when the damage is inflicted by a cell-sucking organism. Here, we present a protocol that allows a non-destructive quantification of the damage inflicted by cell-sucking arthropods, robustly filtering out leaf vascular structures that might be mistakenly classified as damage in many plant species. The protocol is set for the laboratory environment and uses Fiji and ilastik, two free software packages.
Arthropods are often infected with Wolbachia inducing cytoplasmic incompatibility (CI), whereby crosses between uninfected females and infected males yield unviable fertilized offspring. Although ...uninfected females benefit from avoiding mating with Wolbachia‐infected males, this behavior is not always present in host populations and its evolution may hinge upon various factors. Here, we used spider mites to test whether CI could select for mate preference in uninfected females in absence of kin recognition. We found that uninfected females from several field‐derived populations showed no preference for infected or uninfected males, nor evolved a preference after being exposed to CI for 12–15 generations by maintaining uninfected females with both infected and uninfected males (i.e., stable “infection polymorphism”). This suggests that Wolbachia‐mediated mate choice evolution may require very specific conditions in spider mites. However, after experimental evolution, the copulation duration of Wolbachia‐infected control males was significantly higher than that of uninfected control males, but not than that of uninfected males from the “infection polymorphism” regime. This result illustrates how gene flow may oppose Wolbachia‐driven divergence between infected and uninfected hosts in natural populations.
Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in ...response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis.
We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = ‘high’‐performing lines) or substantial (‘low’‐performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex‐specific responses, and to identify candidate genes underlying such variation.
Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females.
We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms.
Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short‐ and long‐term consequences for the evolution of populations in response to a warming world.
Exposing an insect population to increasing heat stress during development, the authors show significant variation in the population for consequences on some, but not all, subsequent adult reproductive traits. This variation is used to identify candidate genes that may underlie thermal fertility limits.
Thermal tolerance range, based on temperatures that result in incapacitating effects, influences species’ distributions and has been used to predict species’ response to increasing temperature. ...Reproductive performance may also be negatively affected at less extreme temperatures, but such sublethal heat-induced sterility has been relatively ignored in studies addressing the potential effects of, and ability of species’ to respond to, predicted climate warming. The few studies examining the link between increased temperature and reproductive performance typically focus on adults, although effects can vary between life history stages. Here we assessed how sublethal heat stress during development impacted subsequent adult fertility and its plasticity, both of which can provide the raw material for evolutionary responses to increased temperature. We quantified phenotypic and genetic variation in fertility of
Drosophila melanogaster
reared at standardized densities in three temperatures (25, 27, and 29°C) from a set of lines of the
Drosophila
Genetic Reference Panel (DGRP). We found little phenotypic variation at the two lower temperatures with more variation at the highest temperature and for plasticity. Males were more affected than females. Despite reasonably large broad-sense heritabilities, a genome-wide association study found little evidence for additive genetic variance and no genetic variants were robustly linked with reproductive performance at specific temperatures or for phenotypic plasticity. We compared results on heat-induced male sterility with other DGRP results on relevant fitness traits measured after abiotic stress and found an association between male susceptibility to sterility and male lifespan reduction following oxidative stress. Our results suggest that sublethal stress during development has profound negative consequences on male adult reproduction, but despite phenotypic variation in a population for this response, there is limited evolutionary potential, either through adaptation to a specific developmental temperature or plasticity in response to developmental heat-induced sterility.
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