Coevolution of species colonisation rates controls food-chain length in spatially structured food webs.

How the complexity of food webs depends on environmental variables is a long-standing ecological question. It is unclear though how food-chain length should vary with adaptive evolution of the constitutive species. Here we model the evolution of species colonisation rates and its consequences on occupancies and food-chain length in metacommunities. When colonisation rates can evolve, longer food-chains can persist. Extinction, perturbation and habitat loss all affect evolutionarily stable colonisation rates, but the strength of the competition-colonisation trade-off has a major role: weaker trade-offs yield longer chains. Although such eco-evo dynamics partly alleviates the spatial constraint on food-chain length, it is no magic bullet: the highest, most vulnerable, trophic levels are also those that least benefit from evolution. We provide qualitative predictions regarding how trait evolution affects the response of communities to disturbance and habitat loss. This highlights the importance of eco-evolutionary dynamics at metacommunity level in determining food-chain length.

A lot of convergence, a bit of divergence: Environment and interspecific interactions shape body colour patterns in Lissotriton newts.

Coexistence with related species poses evolutionary challenges to which populations may react in diverse ways. When exposed to similar environments, sympatric populations of two species may adopt similar phenotypic trait values. However, selection may also favour trait divergence as a way to reduce competition for resources or mates. The characteristics of external body parts, such as coloration and external morphology, are involved to varying degrees in intraspecific signalling as well as in the adaptation to the environment and consequently may be diversely affected by interspecific interactions in sympatry. Here, we studied the effect of sympatry on various colour and morphological traits in males and females of two related newt species Lissotriton helveticus and L. vulgaris. Importantly, we did not only estimate how raw trait differences between species respond to sympatry, but also the marginal responses after controlling for environmental variation. We found that dorsal and caudal coloration converged in sympatry, likely reflecting their role in adaptation to local environments, especially concealment from predators. In contrast, aspects of male and female ventral coloration, which harbours sexual signals in both species, diverged in sympatry. This divergence may reduce opportunities for interspecific sexual interactions and the associated loss of energy, suggesting reproductive character displacement (RCD). Our study emphasizes the contrasting patterns of traits involved in different functions and calls for the need to consider this diversity in evolutionary studies.

Environmental effects on the genetic architecture of fitness components in a simultaneous hermaphrodite.

Understanding how environmental change affects genetic variances and covariances of reproductive traits is key to formulate firm predictions on evolutionary responses. This is particularly true for sex-specific variance in reproductive success, which has been argued to affect how populations can adapt to environmental change. Our current knowledge on the impact of environmental stress on sex-specific genetic architecture of fitness components is still limited and restricted to separate-sexed organisms. However, hermaphroditism is widespread across animals and may entail interesting peculiarities with respect to genetic constraints imposed on the evolution of male and female reproduction. We explored how food restriction affects the genetic variance-covariance (G) matrix of body size and reproductive success of the simultaneously hermaphroditic freshwater snail Physa acuta. Our results provide strong evidence that the imposed environmental stress elevated the opportunity for selection in both sex functions. However, the G-matrix remained largely stable across the tested food treatments. Importantly, our results provide no support for cross-sex genetic correlations suggesting no strong evolutionary coupling of male and female reproductive traits. We discuss potential implications for the adaptation to changing environments and highlight the need for more quantitative genetic studies on male and female fitness components in simultaneous hermaphrodites.

Systematics and geographical distribution of Galba species, a group of cryptic and worldwide freshwater snails.

Cryptic species can present a significant challenge to the application of systematic and biogeographic principles, especially if they are invasive or transmit parasites or pathogens. Detecting cryptic species requires a pluralistic approach in which molecular markers facilitate the detection of coherent taxonomic units that can then be analyzed using various traits (e.g., internal morphology) and crosses. In asexual or self-fertilizing species, the latter criteria are of limited use. We studied a group of cryptic freshwater snails (genus Galba) from the family Lymnaeidae that have invaded almost all continents, reproducing mainly by self-fertilization and transmitting liver flukes to humans and livestock. We aim to clarify the systematics, distribution, and phylogeny of these species with an integrative approach that includes morphology, molecular markers, wide-scale sampling across America, and data retrieved from GenBank (to include Old World samples). Our phylogenetic analysis suggests that the genus Galba originated ca. 22 Myr ago and today comprises six species or species complexes. Four of them show an elongated-shell cryptic phenotype and exhibit wide variation in their genetic diversity, geographic distribution, and invasiveness. The remaining two species have more geographically restricted distributions and exhibit a globose-shell cryptic phenotype, most likely phylogenetically derived from the elongated one. We emphasize that no Galba species should be identified without molecular markers. We also discuss several hypotheses that can explain the origin of cryptic species in Galba, such as convergence and morphological stasis.

How community adaptation affects biodiversity-ecosystem functioning relationships.

Evidence is growing that evolutionary dynamics can impact biodiversity-ecosystem functioning (BEF) relationships. However the nature of such impacts remains poorly understood. Here we use a modelling approach to compare random communities, with no trait evolutionary fine-tuning, and co-adapted communities, where traits have co-evolved, in terms of emerging biodiversity-productivity, biodiversity-stability and biodiversity-invasion relationships. Community adaptation impacted most BEF relationships, sometimes inverting the slope of the relationship compared to random communities. Biodiversity-productivity relationships were generally less positive among co-adapted communities, with reduced contribution of sampling effects. The effect of community-adaptation, though modest regarding invasion resistance, was striking regarding invasion tolerance: co-adapted communities could remain very tolerant to invasions even at high diversity. BEF relationships are thus contingent on the history of ecosystems and their degree of community adaptation. Short-term experiments and observations following recent changes may not be safely extrapolated into the future, once eco-evolutionary feedbacks have taken place.

Assessing metacommunity processes through signatures in spatiotemporal turnover of community composition.

Although metacommunity ecology has been a major field of research in the last decades, with both conceptual and empirical outputs, the analysis of the temporal dynamics of metacommunities has only emerged recently and consists mostly of repeated static analyses. Here we propose a novel analytical framework to assess metacommunity processes using path analyses of spatial and temporal diversity turnovers. We detail the principles and practical aspects of this framework and apply it to simulated datasets to illustrate its ability to decipher the respective contributions of entangled drivers of metacommunity dynamics. We then apply it to four empirical datasets. Empirical results support the view that metacommunity dynamics may be generally shaped by multiple ecological processes acting in concert, with environmental filtering being variable across both space and time. These results reinforce our call to go beyond static analyses of metacommunities that are blind to the temporal part of environmental variability.

Looking for Mimicry in a Snake Assemblage Using Deep Learning.

Batesian mimicry is a canonical example of evolution by natural selection, popularized by highly colorful species resembling unrelated models with astonishing precision. However, Batesian mimicry could also occur in inconspicuous species and rely on subtle resemblance. Although potentially widespread, such instances have been rarely investigated, such that the real frequency of Batesian mimicry has remained largely unknown. To fill this gap, we developed a new approach using deep learning to quantify the visual resemblance between putative mimics and models from photographs. We applied this method to Western Palearctic snakes. Potential nonvenomous mimics were revealed by an excess of resemblance to sympatric venomous snakes compared with random expectations. We found that 8% of the nonvenomous species were potential mimics, although they resembled their models imperfectly. This study is the first to quantify the frequency of Batesian mimicry in a whole community of vertebrates, and it shows that even concealed species can act as potential models. Our approach should prove useful for detecting mimicry in other communities, and more generally it highlights the benefits of deep learning for quantitative studies of phenotypic resemblance.

Do metrics of sexual selection conform to Bateman's principles in a wind-pollinated plant?

Bateman's principles posit that male fitness varies more, and relies more on mate acquisition, than female fitness. While Bateman's principles should apply to any organism producing gametes of variable sizes, their application to plants is potentially complicated by the high levels of polyandry suspected for plants, and by variation in the spatial distribution of prospective mates. Here we quantify the intensity of sexual selection by classical Bateman metrics using two common gardens of the wind-pollinated dioecious plant Mercurialis annua. Consistent with Bateman's principles, males displayed significantly positive Bateman gradients (a regression of fitness on mate number), whereas the reproductive success of females was independent of their ability to access mates. A large part of male fitness was explained by their mate number, which in turn was associated with males' abilities to disperse pollen. Our results suggest that sexual selection can act in plant species in much the same way as in many animals, increasing the number of mates through traits that promote pollen dispersal.

Bioinvasion Triggers Rapid Evolution of Life Histories in Freshwater Snails.

Biological invasions offer interesting situations for observing how novel interactions between closely related, formerly allopatric species may trigger phenotypic evolution in situ. Assuming that successful invaders are usually filtered to be competitively dominant, invasive and native species may follow different trajectories. Natives may evolve traits that minimize the negative impact of competition, while trait shifts in invasives should mostly reflect expansion dynamics, through selection for colonization ability and transiently enhanced mutation load at the colonization front. These ideas were tested through a large-scale common-garden experiment measuring life-history traits in two closely related snail species, one invasive and one native, co-occurring in a network of freshwater ponds in Guadeloupe. We looked for evidence of recent evolution by comparing uninvaded or recently invaded sites with long-invaded ones. The native species adopted a life history favoring rapid population growth (i.e., increased fecundity, earlier reproduction, and increased juvenile survival) that may increase its prospects of coexistence with the more competitive invader. We discuss why these effects are more likely to result from genetic change than from maternal effects. The invader exhibited slightly decreased overall performances in recently colonized sites, consistent with a moderate expansion load resulting from local founder effects. Our study highlights a rare example of rapid life-history evolution following invasion.

Sex-specific strategies of resource allocation in response to competition for light in a dioecious plant.

The differential plasticity hypothesis suggests that sexual dimorphism in dioecious plants could evolve in response to sex-specific resource requirements for reproduction (i.e., high carbon requirements for ovules and high nitrogen demands for pollen). When resources become limiting during growth, males and females should, therefore, adjust their allocation to resource-harvesting organs differently. To investigate the potential for plants to respond to resource limitation late in life and to test the differential plasticity hypothesis, we grew male and female individuals of the annual wind-pollinated plant Mercurialis annua in a common garden. Late in the growth season, we simulated a change in competition by decreasing plant density in half of the replicates. We measured both allocation to vegetative and reproductive traits and analyzed the relative allocation to reproduction vs. growth. Males and females differentially adjusted their resource allocation in response to varying plant densities, despite the fact that they were reproductively mature. Males maintained the same relative allocation of resource to reproductive vs. vegetative tissues at both densities. In contrast, females reduced vegetative growth proportionally less than seed production at the higher density. Our results highlight the dynamic nature of allocation decisions taken by plants, which respond quickly and in a sexually dimorphic way to changes in their competitive circumstances. The existence of resource 'currencies' limiting male and female functions differently have potentially led to the evolution of sex-specific strategies of resource acquisition and deployment, with females conserving resources for vegetative organs to ensure their future carbon-rich reproduction.

High-throughput sequencing reveals inbreeding depression in a natural population.

Proxy measures of genome-wide heterozygosity based on approximately 10 microsatellites have been used to uncover heterozygosity fitness correlations (HFCs) for a wealth of important fitness traits in natural populations. However, effect sizes are typically very small and the underlying mechanisms remain contentious, as a handful of markers usually provides little power to detect inbreeding. We therefore used restriction site associated DNA (RAD) sequencing to accurately estimate genome-wide heterozygosity, an approach transferrable to any organism. As a proof of concept, we first RAD sequenced oldfield mice (Peromyscus polionotus) from a known pedigree, finding strong concordance between the inbreeding coefficient and heterozygosity measured at 13,198 single-nucleotide polymorphisms (SNPs). When applied to a natural population of harbor seals (Phoca vitulina), a weak HFC for parasite infection based on 27 microsatellites strengthened considerably with 14,585 SNPs, the deviance explained by heterozygosity increasing almost fivefold to a remarkable 49%. These findings arguably provide the strongest evidence to date of an HFC being due to inbreeding depression in a natural population lacking a pedigree. They also suggest that under some circumstances heterozygosity may explain far more variation in fitness than previously envisaged.

Molecular Evolution of Freshwater Snails with Contrasting Mating Systems.

Because mating systems affect population genetics and ecology, they are expected to impact the molecular evolution of species. Self-fertilizing species experience reduced effective population size, recombination rates, and heterozygosity, which in turn should decrease the efficacy of natural selection, both adaptive and purifying, and the strength of meiotic drive processes such as GC-biased gene conversion. The empirical evidence is only partly congruent with these predictions, depending on the analyzed species, some, but not all, of the expected effects have been observed. One possible reason is that self-fertilization is an evolutionary dead-end, so that most current selfers recently evolved self-fertilization, and their genome has not yet been strongly impacted by selfing. Here, we investigate the molecular evolution of two groups of freshwater snails in which mating systems have likely been stable for several millions of years. Analyzing coding sequence polymorphism, divergence, and expression levels, we report a strongly reduced genetic diversity, decreased efficacy of purifying selection, slower rate of adaptive evolution, and weakened codon usage bias/GC-biased gene conversion in the selfer Galba compared with the outcrosser Physa, in full agreement with theoretical expectations. Our results demonstrate that self-fertilization, when effective in the long run, is a major driver of population genomic and molecular evolutionary processes. Despite the genomic effects of selfing, Galba truncatula seems to escape the demographic consequences of the genetic load. We suggest that the particular ecology of the species may buffer the negative consequences of selfing, shedding new light on the dead-end hypothesis.

Lower selfing rates in metallicolous populations than in non-metallicolous populations of the pseudometallophyte Noccaea caerulescens (Brassicaceae) in Southern France.

BACKGROUND AND AIMS: The pseudometallophyte Noccaea caerulescens is an excellent model to study evolutionary processes, as it grows both on normal and on heavy-metal-rich, toxic soils. The evolution and demography of populations are critically impacted by mating system and, yet, information about the N. caerulescens mating system is limited. METHODS: Mean selfing rates were assessed using microsatellite loci and a robust estimation method (RMES) in five metallicolous and five non-metallicolous populations of N. caerulescens in Southern France, and this measure was replicated for two successive reproductive seasons. As a part of the study, the patterns of gene flow among populations were analysed. The mating system was then characterized at a fine spatial scale in three populations using the MLTR method on progeny arrays. KEY RESULTS: The results confirm that N. caerulescens has a mixed mating system, with selfing rates ranging from 0·2 to 0·5. Selfing rates did not vary much among populations within ecotypes, but were lower in the metallicolous than in the non-metallicolous ecotype, in both seasons. Effective population size was also lower in non-metallicolous populations. Biparental inbreeding was null to moderate. Differentiation among populations was generally high, but neither ecotype nor isolation by distance explained it. CONCLUSIONS: The consequences of higher selfing rates on adaptation are expected to be weak to moderate in non-metallicolous populations and they are expected to suffer less from inbreeding depression, compared to metallicolous populations.

Environment-Dependent Sexual Selection: Bateman's Parameters under Varying Levels of Food Availability.

Sexual selection is a potent evolutionary force that has been shown to vary in strength and direction depending on demographic factors such as density and sex ratio. However, the effect of other environmental factors on the mode of sexual selection remains largely unexplored. Here, we tested experimentally how food restriction affects the potential for sexual selection in the male and the female sex function of the simultaneously hermaphroditic freshwater snail Physa acuta. We manipulated food availability and compared Bateman's metrics of sexual selection between groups of five well-fed and five food-restricted snails. Food-restricted individuals had a reduced female reproductive output, suggesting that we successfully manipulated the reproductive resources. Importantly, food restriction reduced the male opportunity for sexual selection (in terms of a lowered variance in male mating success) and led to diminishing returns of mating in both sexes (in terms of nonsignificant Bateman gradients). Furthermore, we observed significant changes in the relative contribution of different fitness components, suggesting stronger postcopulatory selection in the male sex role and stronger fecundity selection in the female sex role under restricted food conditions. This study highlights the need to incorporate ecological factors to better understand how sexual selection operates in the wild.

A neutral theory for interpreting correlations between species and genetic diversity in communities.

Spatial patterns of biological diversity have been extensively studied in ecology and population genetics, because they reflect the forces acting on biodiversity. A growing number of studies have found that genetic (within-species) and species diversity can be correlated in space (the so-called species-gene diversity correlation [SGDC]), which suggests that they are controlled by nonindependent processes. Positive SGDCs are generally assumed to arise from parallel responses of genetic and species diversity to variation in site size and connectivity. However, this argument implicitly assumes a neutral model that has yet to be developed. Here, we build such a model to predict SGDC in a metacommunity. We describe how SGDC emerges from competition within sites and variation in connectivity and carrying capacity among sites. We then introduce the formerly ignored mutation process, which affects genetic but not species diversity. When mutation rate is low, our model confirms that variation in the number of migrants among sites creates positive SGDCs. However, when considering high mutation rates, interactions between mutation, migration, and competition can produce negative SGDCs. Neutral processes thus do not always contribute positively to SGDCs. Our approach provides empirical guidelines for interpreting these novel patterns in natura with respect to evolutionary and ecological forces shaping metacommunities.

Multiple invasions and predation: The impact of the crayfish Cherax quadricarinatus on invasive and native snails.

The pace of biological invasions has increased in recent decades, leading to multiple invasions and the potential dominance of invasive species, destabilizing local ecological networks. This provides opportunities to study new ecological species interactions, including predation. Tropical freshwaters have been particularly concerned by aquatic invasions and we focused here on the Martinique island (Lesser Antilles). We examined the predator-prey relationships involving invasive Thiarid snails (Tarebia granifera and Melanoides tuberculata) and the native Neritina punctulata, both confronted with a newcomer predator, the redclaw crayfish (Cherax quadricarinatus). We conducted several mesocosm experiments to assess the impact of crayfish predation on snail survival and the passive and active antipredator responses of snails. A first experiment indicated snail survival rates between 50% and 80%, depending on crayfish size and sex. Notably, there was a negative correlation between snail survival and male crayfish size and the predation method (shell crushing vs. "body sucking") varied with crayfish size. The second experiment suggested no refuge size for snails, with both very small (<5 mm) and very large (>5 mm) unable to escape predation, regardless of crayfish size (from 77 to 138 mm) or sex. Finally, we investigated the escape behavior of Thiarids regarding three crayfish cues. Melanoides tuberculata tend to bury in the substrate and T. granifera to climb up aquarium walls, what was expected from their shell morphologies, and both responding to crayfish cues within minutes. Overall, C. quadricarinatus proves to be an efficient snail predator with limited escape options for snails, potentially contributing to the decline of certain snail populations in Martinique. This omnivorous predator might impact other native species across different groups, including shrimps and fish. Our study underscores the urgent need for monitoring efforts, solidifying the redclaw crayfish reputation as a dangerous invasive species for freshwater macrobenthic faunas worldwide.

Both nuclear and cytoplasmic polymorphisms are involved in genetic conflicts over male fertility in the gynodioecious snail Physa acuta.

Gynodioecy, the coexistence of hermaphrodites with females, often reflects conflicts between cytoplasmic male sterility (CMS) genes and nuclear genes restoring male fertility. CMS is frequent in plants, and has been recently discovered in one animal: the freshwater snail Physa acuta. In this system, CMS was linked to a single divergent mitochondrial genome (D), devoid of apparent nuclear restoration. Our study uncovers a second, novel CMS-associated mitogenome (K) in Physa acuta, demonstrating an extraordinary acceleration of molecular evolution throughout the entire K mitochondrial genome, akin to the previously observed pattern in D. This suggests a pervasive occurrence of accelerated evolution in both CMS-associated lineages. Through a 17-generation introgression experiment, we further show that nuclear polymorphisms in K-mitogenome individuals contribute to the restoration of male function in natural populations. Our results underscore shared characteristics in gynodioecy between plants and animals, emphasizing the presence of multiple CMS mitotypes and cyto-nuclear conflicts. This reaffirms the pivotal role of mitochondria in influencing male function and in generating genomic conflicts that impact reproductive processes in animals.

Metapopulation dynamics of species with cryptic life stages.

Quantifying metapopulation dynamics is a challenging task. Difficulties particularly arise in species that possess unobservable resistance forms that bias the estimation of colonization and persistence rates. Here, we develop a general multistate occupancy model that allows estimation of species persistence for both normal and resistant forms, even when the latter are not detectable. We apply this model to an 11-year data set on the tropical freshwater snail Drepanotrema depressissimum in a network of 229 ponds. These ponds frequently dry out, and the snails can persist by aestivating in the ground, where they are not detected. Our model adequately captures this feature because it infers a high persistence rate for the resistant form, while models ignoring aestivation tend to overestimate extinction and colonization. In addition, we find that, surprisingly, colonization and persistence are even higher in sites prone to desiccation and during years with low rainfall than in more humid sites and years, suggesting that D. depressissimum favors unstable sites where competitors are rare and where it can rely on aestivation to persist. Our model has the potential to provide valuable insights into the metapopulation dynamics of many species that otherwise could hardly be studied because of the existence of undetectable life forms.

Phenotypic plasticity allows the Mediterranean parsley frog Pelodytes punctatus to exploit two temporal niches under continuous gene flow.

Environmental changes, such as climate change, lead to the opening of new niches. In such situations, species that adapt to new niches can survive and/or expand their ranges. However, gene flow can hamper genetic adaptation to new environments. Alternatively, recent models have highlighted the importance of phenotypic plasticity in tracking environmental change. Here, we investigate whether phenotypic plasticity or genetic evolution (or both) allows an amphibian species to exploit two divergent climatic niches. In the Mediterranean region, the parsley frog Pelodytes punctatus breeds both in spring, as do most other species, and in autumn, a temporal niche not exploited by most other species, but which may become increasingly important with global warming. Conditions of development are dramatically different between the two seasons and deeply impact tadpole life-history traits. To determine whether these temporal niches are exploited by two genetically differentiated subpopulations, or whether the bimodal phenology arises in a panmictic population displaying plastic life-history traits, we use two complementary approaches. We measure both molecular genetic differentiation and quantitative-trait differentiation between spring and autumn cohorts, using microsatellites and common garden experiments, respectively. Seasonal cohorts were not genetically differentiated and differences in tadpole life history between cohorts were not maintained in laboratory conditions. We conclude that phenotypic plasticity, rather than genetic adaptation, allows Parsley frog to exploit two contrasting temporal niches.

Rapid divergence in vegetative morphology of a wind-pollinated plant between populations at contrasting densities.

Plant sexual dimorphism is thought to evolve in response to sex-specific selection associated with competition for access to mates or resources, both of which may be density dependent. In wind-pollinated plants in particular, vegetative traits such as plant size and architecture may influence resource acquisition and both pollen dispersal and receipt, with potential conflict between these two components of fitness. We evaluated the role of plant density in shaping plant traits by measuring evolutionary responses in experimental populations of the sexually dimorphic wind-pollinated plant Mercurialis annua. After three generations of evolution, we observed divergence between high- and low-density populations in several vegetative traits, whereas there was no divergence for reproductive traits. A reversal in the direction of sexually dimorphic traits expressed in young plants evolved in both low- and high-density populations compared to the original population (stored as seeds). Compared to the source population, males at high density evolved to be taller when young, whereas at low density young females tended to become smaller. These results demonstrate that a simple change in plant density can induce age-dependent and sex-specific evolution in the ontogeny of vegetative organs, and illustrates the power of experimental evolution for investigating plant trait evolution.