Sex-related Differences in Aging Rate Are Associated with Sex Chromosome System in Amphibians

Sex-related differences in mortality are widespread in the animal kingdom. Although studies have shown that sex determination systems might drive lifespan evolution, sex chromosome influence on aging rates have not been investigated so far, likely due to an apparent lack of demographic data from clades including both XY (with heterogametic males) and ZW (heterogametic females) systems. Taking advantage of a unique collection of capture–recapture datasets in amphibians, a vertebrate group where XY and ZW systems have repeatedly evolved over the past 200 million years, we examined whether sex heterogamy can predict sex differences in aging rates and lifespans. We showed that the strength and direction of sex differences in aging rates (and not lifespan) differ between XY and ZW systems. Sex-specific variation in aging rates was moderate within each system, but aging rates tended to be consistently higher in the heterogametic sex. This led to small but detectable effects of sex chromosome system on sex differences in aging rates in our models. Although preliminary, our results suggest that exposed recessive deleterious mutations on the X/Z chromosome (the “unguarded X/Z effect”) or repeat-rich Y/W chromosome (the “toxic Y/W effect”) could accelerate aging in the heterogametic sex in some vertebrate clades

Context‐dependent dispersal determines relatedness and genetic structure in a patchy amphibian population

Dispersal is a central process in ecology and evolution with far reaching consequences for the dynamics and genetics of spatially structured populations (SSPs). Individuals can adjust their decisions to disperse according to local fitness prospects, resulting in context-dependent dispersal. By determining dispersal rate, distance, and direction, these individual-level decisions further modulate the demography, relatedness, and genetic structure of SSPs. Here, we examined how context-dependent dispersal influences the dynamics and genetics of a Great Crested Newt (Triturus cristatus) SSP. We collected capture-recapture data of 5564 individuals and genetic data of 950 individuals across a SSP in northern Germany. We added genetic data from six sites outside this SSP to assess genetic structure and gene flow at a regional level. Dispersal rates within the SSP were high but dispersal distances were short. Dispersal was context-dependent: individuals preferentially immigrated into high-quality ponds where breeding probabilities were higher. The studied SSP behaved like a patchy population, where subpopulations at each pond were demographically interdependent. High context-dependent dispersal led to weak but significant spatial genetic structure and relatedness within the SSP. At the regional level, a strong hierarchical genetic structure with very few first-generation migrants as well as low effective dispersal rates suggest the presence of independent demographic units. Overall, our study highlights the importance of habitat quality for driving context-dependent dispersal and therefore demography and genetic structure in SSPs. Limited capacity for long-distance dispersal seems to increase genetic structure within a population and leads to demographic isolation in anthropogenic landscapes.Microsatellite Genotypes: Missing values are coded "-9". Presence/Absence Data: Missing values are coded "-". Funding provided by: Deutsche ForschungsgemeinschaftCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001659Award Number: STE 1130/7-1Demographic Data (CMR and Presence/Absence Data): We surveyed 33 water bodies using mark-recapture methods for the presence, demography and reproduction of crested newts between 2012 and 2014. Newts were captured during two capture sessions (cs) per year, one early (April/May) and one late (June/July) in the breeding season. Every capture session thereby consisted of three consecutive capture events in intervals of two days. Within the context of a presence/absence analysis, all sites were surveyed for one more day in late July/early August in order to detect larvae. If a pond dried out and was therefore not surveyed during a capture session, such an event was treated as a missing observation. Newts were captured using Ortmann's funnel traps which were evenly distributed along the shoreline of a pond. The number of traps deployed per capture event varied according to pond perimeter (one trap per 10m shoreline), ranging from one to 27 traps. For individual recognition of newts during the CMR study, we used photographs of the ventral side of an individual which provides a natural marking in form of a highly variable but individually unique and stable color pattern through the time. Recaptured individuals were identified automatically by the software AmphIdent. Microsatellite Genotypes: Tissue samples were taken from seven sampling sites by puncturing the tails of captured great crested newts (Triturus cristatus) using micro haematocrit capillary tubes (Carl Roth, Ø 1.6 mm) and were then stored in 80% ethanol. Total genomic DNA was extracted using the sodium dodecyl sulfate (SDS)-proteinase K/ Phenol-Chloroform extraction method. Genomic DNA was stored in Tris-EDTA buffer (10 mM Tris-HCl, 0.1 mM EDTA, pH 8.0) and used for all subsequent reactions. Each individual sample was mugenotyped for 17 microsatellite loci. Primers were combined in three multiplex mixes (Drechsler et al., 2013). 10 µl Type-it Multiplex PCRs (Qiagen) containing 1 µl of genomic DNA were performed. The PCR profile was as follows: (1) 5 min at 95°C, (2) 30 s at 94°C, (3) 90 s at an annealing temperature of 60°C, (4) 60 s at 72°C, (5) return to step 2 for 30 times, (6) 30 min at 60°C. Obtained PCR products were diluted with 50-200 μl water depending on the strength of obtained PCR products. 1 µl of each diluted multiplex reaction was added to 20 μl of Genescan 500-LIZ size standard (Applied Biosystem) and then run on an ABI 3730 96-capillary or an ABI 3130 16-capillary automated DNA-sequencer. Allele scoring of microsatellite loci was performed using Genemarker software (SoftGenetics version 1.95)

Transgenerational plasticity of dispersal‐related traits in a ciliate: genotype‐dependency and fitness consequences

Phenotypic plasticity, the ability of one genotype to produce different phenotypes in different environments, plays a central role in species' response to environmental changes. Transgenerational plasticity (TGP) allows the transmission of this environmentally-induced phenotypic variation across generations, and can influence adaptation. To date, the genetic control of TGP, its long-term stability, and its potential costs remain largely unknown, mostly because empirical demonstrations of TGP across many generations in several genetic backgrounds are scarce. Here, we examined how genotype determines the TGP of phenotypic traits related to dispersal, a fundamental process in ecology and evolution. We used an experimental approach in Tetrahymena thermophila, a ciliate model-species, to determine if and how phenotypic changes expressed following a dispersal treatment are inherited over multiple generations. Our results show that morphological and movement traits associated with dispersal are plastic, and that these modifications are inherited over at least 35 generations. The fitness costs and benefits associated with these plastic changes are also transmitted to further generations. We highlight that the genotype modulates the expression and reversibility of transgenerational plasticity of dispersal-related traits and its fitness outcomes. Our study thus suggests that genotype-dependent TGP could play an important role in eco-evolutionary dynamics as dispersal determines gene flow and the long-term persistence of natural populations

Asynchrony of actuarial and reproductive senescence: a lesson from an indeterminate grower

International audienceAging evolutionary theories predict that patterns of actuarial and reproductive senescence should be aligned, with a common onset of senescence set at the age of first reproduction. However, a few empirical studies reported asynchrony between actuarial and reproductive senescence. This asynchrony is expected to be particularly pronounced in organisms with indeterminate growth. Yet, this process is still poorly documented due to the lack of long-term demographic data on knownaged individuals. We investigated the asynchrony of actuarial and reproductive senescence in th

Environmentally mediated reproductive success predicts breeding dispersal decisions in an early successional amphibian

Dispersal is a central mechanism in ecology and evolution. Dispersal evolution is driven by a trade-off between costs and benefits, which is influenced by interindividual variability and local environmental conditions (context-dependent dispersal). Many studies have investigated how dispersal decisions may be influenced by environmental factors, including density, predation and interspecific competition. Yet few have attempted to examine how habitat disturbance may affect the dispersal process in spatially structured populations. In early successional species, one might expect individuals to adjust their dispersal decisions based on two main factors that potentially have an influence on reproductive success: patch size and the level of patch disturbance. In this study, we examined how these two factors affect breeding success and dispersal decisions in an early successional amphibian, the yellow- bellied toad, Bombina variegata. To this end, we used capture–recapture data collected on a spatially structured population occupying 28 breeding patches. We took advantage of recent developments in multievent capture–recapture models to detect signs of context-dependent dispersal. The results revealed that the probability of successful reproduction and the number of newly metamorphosed individuals increased with both the size and the proportion of disturbance of a patch. In addition, our results showed that the factors affecting breeding success also influenced breeding dispersal probability. Large patch size negatively influenced emigration probability; in contrast, it positively influenced immigration probability. Equally, higher disturbance had a strong negative influence on emigration probability and slightly positively affected immigration probability. These findings strongly suggest that individuals make context-dependent dispersal decisions, adjusted to maximize future fitness prospects in a patch, allowing them to better cope with rapid changes in environmental conditions resulting from the ecological succession process. This opens new areas of potential research into the role of dispersal in organism specialization along an ecological succession gradient

Kin-dependent dispersal influences relatedness and genetic structuring in a lek system

Kin selection and dispersal play a critical role in the evolution of cooperative breeding systems. Limited dispersal increases relatedness in spatially structured populations (population viscosity), with the result that neighbours tend to be genealogical relatives. Yet the increase in neighbours’ fitness-related performance through altruistic interaction may also result in habitat saturation and thus exacerbate local competition between kin. Our goal was to detect the footprint of kin selection and competition by examining the spatial structure of relatedness and by comparing non-effective and effective dispersal in a population of a lekking bird, Tetrao urogallus. For this purpose, we analysed capture–recapture and genetic data collected over a 6-year period on a spatially structured population of T. urogallus in France. Our findings revealed a strong spatial structure of relatedness in males. They also indicated that the population viscosity could allow male cooperation through two non-exclusive mechanisms. First, at their first lek attendance, males aggregate in a lek composed of relatives. Second, the distance corresponding to non-effective dispersal dramatically outweighed effective dispersal distance, which suggests that dispersers incur high post-settlement costs. These two mechanisms result in strong population genetic structuring in males. In females, our findings revealed a lower level of spatial structure of relatedness and genetic structure in respect to males. Additionally, non-effective dispersal and effective dispersal distances in females were highly similar, which suggests limited post- settlement costs. These results indicate that kin-dependent dispersal decisions and costs have a genetic footprint in wild populations and are factors that may be involved in the evolution of cooperative courtship

Drivers of amphibian population dynamics and asynchrony at local and regional scales

Identifying the drivers of population fluctuations in spatially distinct populations remains a significant challenge for ecologists. Whereas regional climatic factors may generate population synchrony (i.e., the Moran effect), local factors including the level of density-dependence may reduce the level of synchrony. Although divergences in the scaling of population synchrony and spatial environmental variation have been observed, the regulatory factors that underlie such mismatches are poorly understood. Few previous studies have investigated how density-dependent processes and population-specific responses to weather variation influence spatial synchrony at both local and regional scales. We addressed this issue in a pond-breeding amphibian, the great crested newt (Triturus cristatus). We used capture-recapture data collected through long-term surveys in five T. cristatus populations in Western Europe. In all populations – and subpopulations within metapopulations – population size, annual survival and recruitment fluctuated over time. Likewise, there was considerable variation in these demographic rates between populations and within metapopulations. These fluctuations and variations appear to be context-dependent and more related to site-specific characteristics than local or regional climatic drivers. We found a low level of demographic synchrony at both local and regional levels. Weather has weak and spatially variable effects on survival, recruitment and population growth rate. In contrast, density-dependence was a common phenomenon (at least for population growth) in almost all populations and subpopulations. Our findings support the idea that the Moran effect is low in species where the population dynamics more closely depends on local factors (e.g. population density and habitat characteristics) than on large-scale environmental fluctuation (e.g. regional climatic variation). Such responses may have far-reaching consequences for the long-term viability of spatially structured populations and their ability to response to large-scale climatic anomalies

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.Peer reviewe

Elevation and latitude drives structure and tree species composition in Andean forests: Results from a large-scale plot network

Our knowledge about the structure and function of Andean forests at regional scales remains limited. Current initiatives to study forests over continental or global scales still have important geographical gaps, particularly in regions such as the tropical and subtropical Andes. In this study, we assessed patterns of structure and tree species diversity along ~ 4000 km of latitude and ~ 4000 m of elevation range in Andean forests. We used the Andean Forest Network (Red de Bosques Andinos, https://redbosques.condesan.org/) database which, at present, includes 491 forest plots (totaling 156.3 ha, ranging from 0.01 to 6 ha) representing a total of 86,964 identified tree stems ≥ 10 cm diameter at breast height belonging to 2341 identified species, 584 genera and 133 botanical families. Tree stem density and basal area increases with elevation while species richness decreases. Stem density and species richness both decrease with latitude. Subtropical forests have distinct tree species composition compared to those in the tropical region. In addition, floristic similarity of subtropical plots is between 13 to 16% while similarity between tropical forest plots is between 3% to 9%. Overall, plots ~ 0.5-ha or larger may be preferred for describing patterns at regional scales in order to avoid plot size effects. We highlight the need to promote collaboration and capacity building among researchers in the Andean region (i.e., South-South cooperation) in order to generate and synthesize information at regional scale.Fil: Malizia, Agustina. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Blundo, Cecilia Mabel. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Carilla, Julieta. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Osinaga Acosta, Oriana. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Cuesta, Francisco. Universidad de Las Américas; Ecuador. Consorcio para el Desarrollo Sostenible de la Ecorregión Andina; EcuadorFil: Duque, Alvaro. Universidad Nacional de Colombia. Sede Medellín; ColombiaFil: Aguirre, Nikolay. Universidad Nacional de Loja. Centro de Investigaciones Tropicales del Ambiente y la Biodiversidad; EcuadorFil: Aguirre, Zhofre. Universidad Nacional de Loja. Centro de Investigaciones Tropicales del Ambiente y la Biodiversidad; EcuadorFil: Ataroff, Michele. Universidad de Los Andes; VenezuelaFil: Baez, Selene. Escuela Politécnica Nacional; EcuadorFil: Calderón Loor, Marco. Universidad de Las Américas; Ecuador. Deakin University; AustraliaFil: Cayola, Leslie. Herbario Nacional de Bolivia; Bolivia. Missouri Botanical Garden; Estados UnidosFil: Cayuela, Luis. Universidad Rey Juan Carlos; EspañaFil: Ceballos, Sergio Javier. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Cedillo, Hugo. Universidad de Cuenca; EcuadorFil: Farfán Ríos, William. Universidad Nacional de San Antonio Abad del Cusco. Herbario Vargas; PerúFil: Feeley, Kenneth J.. University of Miami; Estados UnidosFil: Fuentes, Alfredo Fernando. Herbario Nacional de Bolivia; Bolivia. Missouri Botanical Garden; Estados UnidosFil: Gámez Álvarez, Luis E.. Universidad de Los Andes; VenezuelaFil: Grau, Hector Ricardo. Universidad Nacional de Tucumán. Instituto de Ecología Regional. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Tucumán. Instituto de Ecología Regional; ArgentinaFil: Homeier, Juergen. Universität Göttingen; AlemaniaFil: Jadan, Oswaldo. Universidad de Cuenca; EcuadorFil: Llambi, Luis Daniel. Escuela Politécnica Nacional; EcuadorFil: Loza Rivera, María Isabel. University of Missouri; Estados Unidos. Herbario Nacional de Bolivia; Bolivia. Missouri Botanical Garden; Estados UnidosFil: Macía, Manuel J.. Universidad Autónoma de Madrid; EspañaFil: Malhi, Yadvinder. University of Oxford; Reino UnidoFil: Malizia, Lucio Ricardo. Universidad Nacional de Jujuy. Facultad de Ciencias Agrarias; ArgentinaFil: Peralvo, Manuel. Consorcio para el Desarrollo Sostenible de la Ecorregión Andina; EcuadorFil: Pinto, Esteban. Consorcio para el Desarrollo Sostenible de la Ecorregión Andina; EcuadorFil: Tello, Sebastián. Missouri Botanical Garden; Estados UnidosFil: Silman, Miles. Center for Energy, Environment and Sustainability; Estados UnidosFil: Young, Kenneth R.. University of Texas at Austin; Estados Unido