The global risk of infectious disease emergence from giant land snail invasion and pet trade.

BACKGROUND: Pathogen outbreaks mostly originate from animals, but some species are more likely to trigger epidemics. The giant land snail (Lissachatina fulica) is a widespread invader, a popular exotic pet, and a notorious vector of the rat lungworm, causing eosinophilic meningitis in humans. However, a comprehensive assessment of the risks of disease outbreak associated with this species is lacking. METHODS: We assessed and mapped the risk of disease transmission associated with the invasion and pet trade of L. fulica. First, we conducted a review of the scientific literature to list all known L. fulica parasites and pathogens and query host-pathogen databases to identify their potential mammalian hosts. Then, to assess the potential for L. fulica to spread globally, we modelled its suitable climatic conditions and tested whether, within climatically suitable areas, the species tended to occur near humans or not. Finally, we used social media data to map L. fulica possession as an exotic pet and to identify human behaviours associated with increased risk of disease transmission. RESULTS: Lissachatina fulica can carry at least 36 pathogen species, including two-thirds that can infect humans. The global invasion of L. fulica is climatically limited to tropical areas, but the species is strongly associated with densely populated areas where snails are more likely to enter in contact with humans. In temperate countries, however, climatic conditions should prevent L. fulica's spread. However, we show that in Europe, giant snails are popular exotic pets and are often handled with direct skin contact, likely increasing the risk of pathogen transmission to their owners. CONCLUSIONS: It is urgent to raise public awareness of the health risks associated with L. fulica in both tropical countries and Europe and to regulate its trade and ownership internationally. Our results highlight the importance of accounting for multiple types of human-wildlife interactions when assessing risks of infectious disease emergence. Furthermore, by targeting the species most likely to spread pathogens, we show that it is possible to rapidly identify emerging disease risks on a global scale, thus guiding timely and appropriate responses.

Sex differences in adult lifespan and aging rate across mammals: A test of the 'Mother Curse hypothesis'.

In many animal species, including humans, males have shorter lifespan and show faster survival aging than females. This differential increase in mortality between sexes could result from the accumulation of deleterious mutations in the mitochondrial genome of males due to the maternal mode of mtDNA inheritance. To date, empirical evidence supporting the existence of this mechanism - called the Mother Curse hypothesis - remains largely limited to a few study cases in humans and Drosophila. In this study, we tested whether the Mother Curse hypothesis accounts for sex differences in lifespan and aging rate across 128 populations of mammals (60 and 68 populations studied in wild and captive conditions, respectively) encompassing 104 species. We found that adult lifespan decreases with increasing mtDNA neutral substitution rate in both sexes in a similar way in the wild - but not in captivity. Moreover, the aging rate marginally increased with neutral substitution rate in males and females in the wild. Overall, these results indicate that the Mother Curse hypothesis is not supported across mammals. We further discuss the implication of these findings for our understanding of the evolution of sex differences in mortality and aging.

Reliability of social media data in monitoring the global pet trade in ants.

The global pet trade is a major risk to biodiversity and humans and has become increasingly globalized, diversified, digitalized, and extremely difficult to control. With billions of internet users posting online daily, social media could be a powerful surveillance tool. But it is unknown how reliably social media can track the global pet trade. We tested whether Instagram data predicted the geographic distribution of pet stores and the taxonomic composition of traded species in the emerging pet trade in ants (Hymenoptera, Formicidae). We visited 138 online stores selling ants as pets worldwide and recorded the species traded. We scraped ∼38,000 Instagram posts from ∼6300 users referencing ants as pets and analyzed comments on post and geolocation (available for ∼1800 users). We tested whether the number of Instagram users predicted the number of ant sellers per country and whether the species referenced as pets on Instagram matched the species offered in online stores, with a particular focus on invasive species. The location of Instagram users referencing ants as pets predicted the location of ant sellers across the globe (R2  = 0.87). Instagram data detected 439 of the 631 ant species traded in online stores (70%), including 59 of the 68 invasive species traded (87%). The number of Instagram users referencing a species was a good predictor of the number of sellers offering the species (R2  = 0.77). Overall, Instagram data provided affordable and reliable data for monitoring the emerging pet trade in ants. Easier access to these data would facilitate monitoring of the global pet trade and help implement relevant regulations in a timely manner.

El mercado global de mascotas es una amenaza importante para la biodiversidad y los humanos y cada vez está más globalizado, diversificado, digitalizado y muy difícil de controlar. Con miles de millones de usuarios publicando a diario en línea, las redes sociales podrían ser una herramienta poderosa de vigilancia, aunque no se sabe cuán confiable puede ser su rastreo del mercado global de mascotas. Analizamos si los datos de Instagram pronosticaban la distribución geográfica de las tiendas de mascotas y la composición taxonómica de las especies comercializadas en el mercado emergente de hormigas mascotas (Hymenoptera, Formicidae). Visitamos 138 tiendas virtuales dedicadas al comercio de hormigas como mascotas a nivel mundial y registramos las especies comercializadas. Reunimos ∼38,000 publicaciones de Instagram de ∼6,300 usuarios que mencionaban a las hormigas como mascotas y analizamos los comentarios en las publicaciones y la geolocalización (disponible para ∼1,800 usuarios). Analizamos si el número de usuarios de Instagram pronosticaba el número de vendedores de hormigas por país y si las especies mencionadas como mascotas en Instagram eran las mismas que aquellas ofrecidas en las tiendas en línea, con foco particular sobre las especies invasoras. La ubicación de los usuarios de Instagram que mencionaban a las hormigas como mascotas pronosticó la ubicación de los vendedores de hormigas alrededor del mundo (R2 = 0.87). La información de Instagram detectó 439 de las 631 especies de hormigas comercializadas en las tiendas virtuales (70%), incluidas 59 de las 68 especies invasoras comercializadas (87%). El número de usuarios de Instagram que mencionaba a una especie fue un buen indicador del número de vendedores que ofrecían esa eespecie (R2 = 0.77). En general, la información de Instagram proporcionó datos accesibles y confiables para el monitoreo del mercado emergente de hormigas mascotas. Un acceso más sencillo a estos datos facilitaría el monitoreo del mercado global de mascotas y ayudaría a implementar regulaciones relevantes de manera oportuna.

Compensatory recruitment allows amphibian population persistence in anthropogenic habitats.

Habitat anthropization is a major driver of global biodiversity decline. Although most species are negatively affected, some benefit from anthropogenic habitat modifications by showing intriguing life-history responses. For instance, increased recruitment through higher allocation to reproduction or improved performance during early-life stages could compensate for reduced adult survival, corresponding to "compensatory recruitment". To date, evidence of compensatory recruitment in response to habitat modification is restricted to plants, limiting understanding of its importance as a response to global change. We used the yellow-bellied toad (Bombina variegata), an amphibian occupying a broad range of natural and anthropogenic habitats, as a model species to test for and to quantify compensatory recruitment. Using an exceptional capture-recapture dataset composed of 21,714 individuals from 67 populations across Europe, we showed that adult survival was lower, lifespan was shorter, and actuarial senescence was higher in anthropogenic habitats, especially those affected by intense human activities. Increased recruitment in anthropogenic habitats fully offset reductions in adult survival, with the consequence that population growth rate in both habitat types was similar. Our findings indicate that compensatory recruitment allows toad populations to remain viable in human-dominated habitats and might facilitate the persistence of other animal populations in such environments.

Genomic signatures of thermal adaptation are associated with clinal shifts of life history in a broadly distributed frog.

Temperature is a critical driver of ectotherm life-history strategies, whereby a warmer environment is associated with increased growth, reduced longevity and accelerated senescence. Increasing evidence indicates that thermal adaptation may underlie such life-history shifts in wild populations. Single nucleotide polymorphisms (SNPs) and copy number variants (CNVs) can help uncover the molecular mechanisms of temperature-driven variation in growth, longevity and senescence. However, our understanding of these mechanisms is still limited, which reduces our ability to predict the response of non-model ectotherms to global temperature change. In this study, we examined the potential role of thermal adaptation in clinal shifts of life-history traits (i.e. life span, senescence rate and recruitment) in the Columbia spotted frog Rana luteiventris along a broad temperature gradient in the western United States. We took advantage of extensive capture-recapture datasets of 20,033 marked individuals from eight populations surveyed annually for 14-18 years to examine how mean annual temperature and precipitation influenced demographic parameters (i.e. adult survival, life span, senescence rate, recruitment and population growth). After showing that temperature was the main climatic predictor influencing demography, we used RAD-seq data (50,829 SNPs and 6,599 putative CNVs) generated for 352 individuals from 31 breeding sites to identify the genomic signatures of thermal adaptation. Our results showed that temperature was negatively associated with annual adult survival and reproductive life span and positively associated with senescence rate. By contrast, recruitment increased with temperature, promoting the long-term viability of most populations. These temperature-dependent demographic changes were associated with strong genomic signatures of thermal adaptation. We identified 148 SNP candidates associated with temperature including three SNPs located within protein-coding genes regulating resistance to cold and hypoxia, immunity and reproduction in ranids. We also identified 39 CNV candidates (including within 38 transposable elements) for which normalized read depth was associated with temperature. Our study indicates that both SNPs and structural variants are associated with temperature and could eventually be found to play a functional role in clinal shifts in senescence rate and life-history strategies in R. luteiventris. These results highlight the potential role of different sources of molecular variation in the response of ectotherms to environmental temperature variation in the context of global warming.

Thermal conditions predict intraspecific variation in senescence rate in frogs and toads.

Variation in temperature is known to influence mortality patterns in ectotherms. Even though a few experimental studies on model organisms have reported a positive relationship between temperature and actuarial senescence (i.e., the increase in mortality risk with age), how variation in climate influences the senescence rate across the range of a species is still poorly understood in free-ranging animals. We filled this knowledge gap by investigating the relationships linking senescence rate, adult lifespan, and climatic conditions using long-term capture-recapture data from multiple amphibian populations. We considered two pairs of related anuran species from the Ranidae (Rana luteiventris and Rana temporaria) and Bufonidae (Anaxyrus boreas and Bufo bufo) families, which diverged more than 100 Mya and are broadly distributed in North America and Europe. Senescence rates were positively associated with mean annual temperature in all species. In addition, lifespan was negatively correlated with mean annual temperature in all species except A. boreas In both R. luteiventris and A. boreas, mean annual precipitation and human environmental footprint both had negligible effects on senescence rates or lifespans. Overall, our findings demonstrate the critical influence of thermal conditions on mortality patterns across anuran species from temperate regions. In the current context of further global temperature increases predicted by Intergovernmental Panel on Climate Change scenarios, a widespread acceleration of aging in amphibians is expected to occur in the decades to come, which might threaten even more seriously the viability of populations and exacerbate global decline.

Insect and plant invasions follow two waves of globalisation.

Globalisation has facilitated the spread of alien species, and some of them have significant impacts on biodiversity and human societies. It is commonly thought that biological invasions have accelerated continuously over the last centuries, following increasing global trade. However, the world experienced two distinct waves of globalisation (~1820-1914, 1960-present), and it remains unclear whether these two waves have influenced invasion dynamics of many species. To test this, we built a statistical model that accounted for temporal variations in sampling effort. We found that insect and plant invasion rates did not continuously increase over the past centuries but greatly fluctuated following the two globalisation waves. Our findings challenge the idea of a continuous acceleration of alien species introductions and highlight the association between temporal variations in trade openness and biological invasion dynamics. More generally, this emphasises the urgency of better understanding the subtleties of socio-economic drivers to improve predictions of future invasions.

Invasiveness is linked to greater commercial success in the global pet trade.

The pet trade has become a multibillion-dollar global business, with tens of millions of animals traded annually. Pets are sometimes released by their owners or escape, and can become introduced outside of their native range, threatening biodiversity, agriculture, and health. So far, a comprehensive analysis of invasive species traded as pets is lacking. Here, using a unique dataset of 7,522 traded vertebrate species, we show that invasive species are strongly overrepresented in trade across mammals, birds, reptiles, amphibians, and fish. However, it is unclear whether this occurs because, over time, pet species had more opportunities to become invasive, or because invasive species have a greater commercial success. To test this, we focused on the emergent pet trade in ants, which is too recent to be responsible for any invasions so far. Nevertheless, invasive ants were similarly overrepresented, demonstrating that the pet trade specifically favors invasive species. We show that ant species with the greatest commercial success tend to have larger spatial distributions and more generalist habitat requirements, both of which are also associated with invasiveness. Our findings call for an increased risk awareness regarding the international trade of wildlife species as pets.

Demography, genetics, and decline of a spatially structured population of lekking bird.

Understanding the mechanisms underlying population decline is a critical challenge for conservation biologists. Both deterministic (e.g. habitat loss, fragmentation, and Allee effect) and stochastic (i.e. demographic and environmental stochasticity) demographic processes are involved in population decline. Simultaneously, a decrease of population size has far-reaching consequences for genetics of populations by increasing the risk of inbreeding and the strength of genetic drift, which together inevitably results in a loss of genetic diversity and a reduced effective population size ([Formula: see text]). These genetic factors may retroactively affect vital rates (a phenomenon coined 'inbreeding depression'), reduce population growth, and accelerate demographic decline. To date, most studies that have examined the demographic and genetic processes driving the decline of wild populations have neglected their spatial structure. In this study, we examined demographic and genetic factors involved in the decline of a spatially structured population of a lekking bird, the western capercaillie (Tetrao urogallus). To address this issue, we collected capture-recapture and genetic data over a 6-years period in the Vosges Mountains (France). Our study showed that the population of T. urogallus experienced a severe decline between 2010 and 2015. We did not detect any Allee effect on survival and recruitment. By contrast, individuals of both sexes dispersed to avoid small subpopulations, thus suggesting a potential behavioral response to a mate finding Allee effect. In parallel to this demographic decline, the population showed low levels of genetic diversity, high inbreeding and low effective population sizes at both subpopulation and population levels. Despite this, we did not detect evidence of inbreeding depression: neither adult survival nor recruitment were affected by individual inbreeding level. Our study underlines the benefit from combining demographic and genetic approaches to investigate processes that are involved in population decline.

Increased acclimation ability accompanies a thermal niche shift of a recent invasion.

Globalization is removing dispersal barriers for the establishment of invasive species and enabling their spread to novel climates. New thermal environments in the invaded range will be particularly challenging for ectotherms, as their metabolism directly depends on environmental temperature. However, we know little about the role climatic niche shifts play in the invasion process, and the underlining physiological mechanisms. We tested if a thermal niche shift accompanies an invasion, and if native and introduced populations differ in their ability to acclimate thermal limits. We used an alien ant species-Tapinoma magnum-which recently started to spread across Europe. Using occurrence data and accompanying climatic variables, we measured the amount of overlap between thermal niches in the native and invaded range. We then experimentally tested the acclimation ability in native and introduced populations by incubating T. magnum at 18, 25 and 30°C. We measured upper and lower critical thermal limits after 7 and 21 days. We found that T. magnum occupies a distinct thermal niche in its introduced range, which is on average 3.5°C colder than its native range. Critical thermal minimum did not differ between populations from the two ranges when colonies were maintained at 25 or 30°C, but did differ after colony acclimation at a lower temperature. We found twofold greater acclimation ability of introduced populations to lower temperatures, after prolonged incubation at 18°C. Increased acclimation ability of lower thermal limits could explain the expansion of the realized thermal niche in the invaded range, and likely contributed to the spread of this species to cooler climates. Such thermal plasticity could be an important, yet so far understudied, factor underlying the expansion of invasive insects into novel climates.