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.

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.

Rapid evolution of pollen and pistil traits as a response to sexual selection in the post-pollination phase of mating.

Sexual selection is the basis of some of the most striking phenotypic variation in nature.1,2 In animals, sexual selection in males can act on traits that improve access to mates prior to copulation,3-8 but also on sperm traits filtered by sperm competition,9-14 or female choice expressed simply by the morphology and physiology of genital tracts.14-16 Although long overlooked as a mode of selection on plant traits, sexual selection should act on land plants too because they are anisogamous: males produce more, and smaller, gametes than females.17-19 Numerical asymmetry in gamete production is thought to play a central role in selection on traits that affect pollen transfer to mates,20,21 but very little is known about how pollen competition or cryptic female choice might affect the evolution of traits expressed after pollination.22,23 Here, we report the divergence of pollen and pistil traits of the dioecious wind-pollinated annual herb Mercurialis annua during evolution over three generations between populations at low versus high plant density, corresponding to low versus higher levels of polyandry;24 we expected selection under higher polyandry to strengthen competition among pollen donors for fertilizing ovules. We found that populations at high density evolved faster-growing pollen tubes (an equivalent of greater sperm velocity), greater expression of pollen proteins involved in pollen growth, and larger stigmas (a trait likely enhancing the number of pollen donors and thus competition for ovules). Our results identify the post-pollination phase of plant mating as an important arena for the action of sexual selection.

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.

Extreme mitochondrial DNA divergence underlies genetic conflict over sex determination.

Cytoplasmic male sterility (CMS) is a form of genetic conflict over sex determination that results from differences in modes of inheritance between genomic compartments.1-3 Indeed, maternally transmitted (usually mitochondrial) genes sometimes enhance their transmission by suppressing the male function in a hermaphroditic organism to the detriment of biparentally inherited nuclear genes. Therefore, these hermaphrodites become functionally female and may coexist with regular hermaphrodites in so-called gynodioecious populations.3 CMS has been known in plants since Darwin's times4 but is previously unknown in the animal kingdom.5-8 We relate the first observation of CMS in animals. It occurs in a freshwater snail population, where some individuals appear unable to sire offspring in controlled crosses and show anatomical, physiological, and behavioral characters consistent with a suppression of the male function. Male sterility is associated with a mitochondrial lineage that underwent a spectacular acceleration of DNA substitution rates, affecting the entire mitochondrial genome-this acceleration concerns both synonymous and non-synonymous substitutions and therefore results from increased mitogenome mutation rates. Consequently, mitochondrial haplotype divergence within the population is exceptionally high, matching that observed between snail taxa that diverged 475 million years ago. This result is reminiscent of similar accelerations in mitogenome evolution observed in plant clades where gynodioecy is frequent,9,10 both being consistent with arms-race evolution of genome regions implicated in CMS.11,12 Our study shows that genomic conflicts can trigger independent evolution of similar sex-determination systems in plants and animals and dramatically accelerate molecular evolution.

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.

The methylome of Biomphalaria glabrata and other mollusks: enduring modification of epigenetic landscape and phenotypic traits by a new DNA methylation inhibitor.

BACKGROUND: 5-Methylcytosine (5mC) is an important epigenetic mark in eukaryotes. Little information about its role exists for invertebrates. To investigate the contribution of 5mC to phenotypic variation in invertebrates, alteration of methylation patterns needs to be produced. Here, we apply new non-nucleoside DNA methyltransferase inhibitors (DNMTi) to introduce aleatory changes into the methylome of mollusk species. RESULTS: Flavanone inhibitor Flv1 was efficient in reducing 5mC in the freshwater snails Biomphalaria glabrata and Physa acuta, and to a lesser degree, probably due to lower stability in sea water, in the oyster Crassostrea gigas. Flv1 has no toxic effects and significantly decreased the 5mC level in the treated B. glabrata and in its offspring. Drug treatment triggers significant variation in the shell height in both generations. A reduced representation bisulfite-sequencing method called epiGBS corroborates hypomethylation effect of Flv1 in both B. glabrata generations and identifies seven Differential Methylated Regions (DMR) out of 32 found both in Flv1-exposed snails and its progeny, from which 5 were hypomethylated, demonstrating a multigenerational effect. By targeted bisulfite sequencing, we confirmed hypomethylation in a locus and show that it is associated with reduced gene expression. CONCLUSIONS: Flv1 is a new and efficient DNMTi that can be used to induce transient and heritable modifications of the epigenetic landscape and phenotypic traits in mollusks, a phylum of the invertebrates in which epigenetics is understudied.

The Scope for Postmating Sexual Selection in Plants.

Sexual selection is known to shape plant traits that affect access to mates during the pollination phase, but it is less well understood to what extent it affects traits relevant to interactions between pollen and pistils after pollination. This is surprising, because both of the two key modes of sexual selection, male-male competition and female choice, could plausibly operate during pollen-pistil interactions where physical male-female contact occurs. Here, we consider how the key processes of sexual selection might affect traits involved in pollen-pistil interactions, including 'Fisherian runaway' and 'good-genes' models. We review aspects of the molecular and cellular biology of pollen-pistil interactions on which sexual selection could act and point to research that is needed to investigate them.

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.

Case report of abdominal left upper quadrant collection secondary to fish bone perforation.

We present an unusual case of an intra-abdominal collection which evidenced a rare etiology and raises diagnostic particularities. BACKGROUND: Fish bones ingestion is frequent, but seldom followed by complications. Those are often reported at specific sites. OBJECTIVES: This case report emphasizes the unusual presentation and site localization of a colonic perforation by a small fish bone, in the context of limited radiological accuracy at the diagnostic phase. CASE PRESENTATION: A 37 year old male was admitted to the gastroenterology ward with upper and left sided abdominal pain associated with fever and marked fatigue. His medical history was marked by a sleeve gastrectomy in 2010 for obesity. Abdominal signs and elevated acute inflammatory syndrome on blood tests were followed by computer tomography which revealed a pericolic mass near the left splenic flexure. The pain and fever increased in intensity, so a laparotomy was proposed. Intraoperatively, a tumor-like lesion was found and a resection with oncologic limits was performed. Microscopic examination of the specimen revealed a fish bone, but only after surgery did the patient confirm that he had eaten fish meal the week before. The post-operative period was uneventful. CONCLUSION: Fish bones remain some of the most frequently ingested alimentary foreign bodies; they may cause atypical clinical presentations, frequently omitted by the patients themselves if symptoms appear delayed. They could also lead to possible high-risk complications which need to be addressed by surgeons.

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.

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.

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.

A simple ATAC-seq protocol for population epigenetics.

We describe here a protocol for the generation of sequence-ready libraries for population epigenomics studies. The protocol is a streamlined version of the Assay for transposase accessible chromatin with high-throughput sequencing (ATAC-seq) that provides a positive display of accessible, presumably euchromatic regions. The protocol is straightforward and can be used with small individuals such as daphnia and schistosome worms, and probably many other biological samples of comparable size, and it requires little molecular biology handling expertise.

Epigenetic inheritance and intergenerational effects in mollusks.

Recent insights in evolutionary biology have shed light on epigenetic variation that interacts with genetic variation to convey heritable information. An important characteristic of epigenetic changes is that they can be produced in response to environmental cues and passed on to later generations, potentially facilitating later genetic adaptation. While our understanding of epigenetic mechanisms in vertebrates is rapidly growing, our knowledge about invertebrates remains lower, or is restricted to model organisms. Mollusks in particular, are a large group of invertebrates, with several species important for ecosystem function, human economy and health. In this review, we attempt to summarize the literature on epigenetic and intergenerational studies in mollusk species, with potential importance for adaptive evolution. Our review highlights that two molecular bearers of epigenetic information, DNA methylation and histone modifications, are key features for development in mollusk species, and both are sensitive to environmental conditions to which developing individuals are exposed. Further, although studies are still scarce, various environmental factors (e.g. predator cues, chemicals, parasites) can induce intergenerational effects on the phenotype (life-history traits, morphology, behaviour) of several mollusk taxa. More work is needed to better understand whether environmentally-induced changes in DNA methylation and histone modifications have phenotypic impacts, whether they can be inherited through generations and their role in intergenerational effects on phenotype. Such work may bring insights into the potential role of epigenetic in adaptation and evolution in mollusks.

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.

Modeling competition, niche, and coexistence between an invasive and a native species in a two-species metapopulation.

Modeling the dynamics of competition and coexistence between species is crucial to predict long-term impacts of invasive species on their native congeners. However, natural environments are often fragmented and variable in time and space. In such contexts, regional coexistence depends on complex interactions between competition, niche differentiation and stochastic colonization-extinction dynamics. Quantifying all these processes at landscape scale has always been a challenge for ecologists. We propose a new statistical framework to evaluate metapopulation parameters (colonization and extinction) in a two-species system and how they respond to environmental variables and interspecific competition. It requires spatial surveys repeated in time, but does not assume demographic equilibrium. We apply this model to a long-term survey of two snails inhabiting a network of freshwater habitats in the West Indies. We find evidence of reciprocal competition affecting colonization or extinction rates, modulated by species-specific sensitivity to environmental variables. Simulations using model estimates allow us to predict species dynamics and explore the role of various coexistence mechanisms described by metacommunity theory in our system. The two species are predicted to stably coexist, because niche partitioning, source-sink dynamics and interspecific differences in extinction-colonization parameters all contribute to reduce the negative impacts of competition. However, none of these mechanisms is individually essential. Regional coexistence is primarily facilitated by transient co-occurrence of the two species within habitat patches, a possibility generally not considered in theoretical metacommunity models. Our framework is general and could be extended to guilds of several competing species.

Sex-specific selection on plant architecture through "budget" and "direct" effects in experimental populations of the wind-pollinated herb, Mercurialis annua.

Sexual selection may contribute to the evolution of plant sexual dimorphism by favoring architectural traits in males that improve pollen dispersal to mates. In both sexes, larger individuals may be favored by allowing the allocation of more resources to gamete production (a "budget" effect of size). In wind-pollinated plants, large size may also benefit males by allowing the liberation of pollen from a greater height, fostering its dispersal (a "direct" effect of size). To assess these effects and their implications for trait selection, we measured selection on plant morphology in both males and females of the wind-pollinated dioecious herb Mercurialis annua in two separate experimental common gardens at contrasting density. In both gardens, selection strongly favored males that disperse their pollen further. Selection for pollen production was observed in the high-density garden only, and was weak. In addition, male morphologies associated with increased mean pollen dispersal differed between the two gardens, as elongated branches were favored in the high-density garden, whereas shorter plants with longer inflorescence stalks were favored in the low-density garden. Larger females were selected in both gardens. Our results point to the importance of both a direct effect of selection on male traits that affect pollen dispersal, and, to a lesser extent, a budget effect of selection on pollen production.