História da colonização do ratinho-caseiro, Mus musculus domesticus, em ilhas AtLânticas (Madeira, Açores e Cabo Verde): uma abordagem multilocus

Tese de mestrado, Biologia Evolutiva e do Desenvolvimento, Universidade de Lisboa, Faculdade de Ciências, 2017As ilhas oceânicas são consideradas laboratórios naturais para o estudo da evolução. Os humanos são também agentes de colonização de várias espécies, nomeadamente, mamíferos terrestres, ao transportarem, ativa ou passivamente, estes animais para as ilhas. Uma das introduções mediadas pelo Homem mais icónicas envolve a disseminação mundial do ratinho-caseiro, principalmente da sub-espécie Mus musculus domesticus, com a qual desenvolveu uma associação comensal, iniciada com o a sedentarização humana há 15000 anos. Esta associação permitiu que o ratinho-caseiro quebrasse todas as barreiras geográficas e atingisse as ilhas oceânicas, aquando das primeiras expansões marítimas, colonizando-as. Neste estudo, foi abordada a colonização desta sub-espécie nos arquipélagos da Macaronésia (Madeira, Açores e Cabo Verde) de colonização histórica portuguesa, através de marcadores moleculares de transmissão exclusivamente materna (D-loop, mtDNA), exclusivamente paterna (microssatélites – cromossoma Y) e bi-parental (intrão Ocrl – cromossoma X), numa abordagem filogeográfica. A análise dos vários marcadores permitiu avaliar a origem da colonização inicial através do mtDNA e seguir possíveis vagas secundárias de colonização através da dispersão diferencial de machos e fêmeas. Os resultados obtidos para o marcador D-loop permitiram reforçar a hipótese de que os países do Norte da Europa constituem a fonte provável de colonização do arquipélago da Madeira. Na ilha da Madeira, para os microssatélites do cromossoma Y, foi detetada uma associação a Portugal continental, que se considera posterior à primeira colonização da ilha. Este sinal de machos com uma origem possivelmente diferente da primeira colonização levou à divergência das ilhas da Madeira e Porto Santo para este marcador. O arquipélago dos Açores reflete na sua maioria a ligação histórica, a Portugal continental, numa colonização inicial. Porém, as ilhas de São Jorge e Santa Maria representam uma exceção ao nível do marcador mitocondrial (já descrita) que é agora refletido também para o cromossoma Y, neste estudo. Este padrão aponta para uma colonização diferente destas ilhas em relação às restantes ilhas do arquipélago dos Açores e entre si.. No arquipélago de Cabo Verde, a análise da população da Ilha de Santa Luzia originou padrões diferentes em cada marcador, tendo sido sugerida uma primeira colonização oriunda das populações residentes da ilha da Madeira, à qual se seguiram várias ondas de colonização. A utilização conjunta dos diferentes marcadores moleculares permitiu avançar no conhecimento da história da colonização do ratinho-caseiro nas ilhas estudadas, mas revelou um cenário bastante complexo e de difícil interpretação em algumas delas, principalmente pela falta de dados para algumas áreas geográficas que poderão ter funcionado como fonte colonizadora. A ligação a Portugal continental, país de onde partiram os descobridores e colonizadores destas ilhas, surge na colonização inicial da maioria das ilhas dos Açores, mas também numa colonização secundária no arquipélago da Madeira, reforçando a ocorrência de uma passagem anterior à portuguesa por esta ilha. Por último, a colonização de Santa Luzia sugere uma colonização inicial através de indivíduos com origem no arquipélago da Madeira, refletindo no entanto, um segundo sinal de colonização de machos com associação à ilha de Santa Maria. Este cenário prevê um padrão de colonização complexo para o arquipélago de Cabo Verde, sendo que esta ilha deve refletir, pelo menos em parte, o padrão das ilhas adjacentes devido à sua utilização como porto piscatório.Oceanic islands are considered natural laboratories for the study of evolution. Humans are also colonizing agents for several species, mainly terrestrial mammals, by actively or passively transporting the animals to the islands. One example of species introduction mediated by humans is the worldwide dissemination of the house mouse, most notably of the subspecies Mus musculus domesticus, with which it developed a commensal relationship that began 15.000 years ago. This relationship allowed the house mouse to overcome all geographic barriers and colonize oceanic islands, ever since the beginning of the European maritime expansion. The present study focuses on the colonization history of the house mouse in the Macaronesian archipelagos historically colonized by the Portuguese (Madeira, Azores and Cape Verde) under a phylogeographic approach. To accomplish this, different molecular markers: exclusively maternal inheritance (D-loop, mtDNA), exclusively paternal inheritance (microsatellites – Y chromosome) and biparental inheritance (Ocrl intron – X chromosome). The overall analysis of the different markers allowed the inference of the origin of the initial colonization through the mtDNA analysis and the identification of possible secondary routes of colonization through the results of the X and Y chromosome markers, allowing the assessment of the differential dispersion of males and females. The results obtained for the D-loop reinforced that Northern European countries are the most likely source of initial colonization of the Madeira archipelago. From the microsatellites of the Y chromosome it was detected an association between Madeira and mainland Portugal, which was interpreted as the result of secondary colonization events. These male-inherited markers also revealed a separation between the Madeira and Porto Santo islands. The Azores archipelago displays, in its majority, the historical connection to mainland Portugal through the initial wave of colonization. However, São Jorge and Santa Maria islands represent an exception at the level of the mitochondrial marker (previously described), which was also observed in this study for the Y chromosome markers. This pattern points towards the possibility of a different wave of colonization of these island, separate from the colonization of the rest of the archipelago. In the Cape Verde archipelago, the analysis of the population from the Santa Luzia island originated different patterns for each marker, which led to the suggestion of a first wave of colonization from the populations occupying Madeira, followed by several secondary waves of colonization. The joint analysis of the different molecular markers contributed to advances in the knowledge of the dissemination, throughout history, of the house mouse in the studied archipelagos. However, in some islands it revealed a very complex scenario of difficult interpretation, especially due to the scarcity of data for some of the geographical areas that may have contributed as colonization sources. The connection to mainland Portugal, the historical discoverer and colonizer, arises in the initial colonization of most Azorean islands but also in a secondary colonization of the Madeira archipelago, reflecting the posterior and continuous presence of the Portuguese over the centuries. Finally, the colonization of Santa Luzia suggests an initial colonization through individuals originated from the Madeira archipelago, showing, nonetheless, a signal of male colonization associated with Santa Maria island. This scenario predicts a complex pattern of colonization of the Cape Verde archipelago, as the results for Santa Luzia seem to be somewhat reflecting the diversity patterns of the adjacent islands

Beneficial developmental acclimation in reproductive performance under cold but not heat stress

Thermal plasticity can help organisms coping with climate change. In this study, we analyse how laboratory populations of the ectotherm species Drosophila subobscura, originally from two distinct latitudes and evolving for several generations in a stable thermal environment (18 °C), respond plastically to new thermal challenges. We measured adult performance (fecundity traits as a fitness proxy) of the experimental populations when exposed to five thermal regimes, three with the same temperature during development and adulthood (15-15 °C, 18-18 °C, 25-25 °C), and two where flies developed at 18 °C and were exposed, during adulthood, to either 15 °C or 25 °C. Here, we test whether (1) flies undergo stress at the two more extreme temperatures; (2) development at a given temperature enhances adult performance at such temperature (i.e. acclimation), and (3) populations with different biogeographical history show plasticity differences. Our findings show (1) an optimal performance at 18 °C only if flies were subjected to the same temperature as juveniles and adults; (2) the occurrence of developmental acclimation at lower temperatures; (3) detrimental effects of higher developmental temperature on adult performance; and (4) a minor impact of historical background on thermal response. Our study indicates that thermal plasticity during development may have a limited role in helping adults cope with warmer - though not colder - temperatures, with a potential negative impact on population persistence under climate change. It also emphasizes the importance of analysing the impact of temperature on all stages of the life cycle to better characterize the thermal limits.info:eu-repo/semantics/publishedVersio

High developmental temperature leads to low reproduction despite adult temperature

Phenotypic plasticity can help organisms cope with changing thermal conditions and it may depend on which life-stage the thermal stress is imposed: for instance, exposure to stressful temperatures during development can trigger a positive plastic response in adults. Here, we analyze the thermal plastic response of laboratory populations of Drosophila subobscura, derived from two contrasting latitudes of the European cline. We measured reproductive performance through fecundity characters, after the experimental populations were exposed to five thermal treatments, with different combinations of developmental and adult temperatures (14°C, 18°C, or 26°C). Our questions were whether (1) adult performance is changed with exposure to higher (or lower) temperatures during development; (2) flies raised at lower temperatures outperform those developed at higher ones, supporting the “colder is better” hypothesis; (3) there is a cumulative effect on adult performance of exposing both juveniles and adults to higher (or lower) temperatures; (4) there is evidence for biogeographical effects on adult performance. Our main findings were that (1) higher developmental temperatures led to low reproductive performance regardless of adult temperature, while at lower temperatures reduced performance only occurred when colder conditions were persistent across juvenile and adult stages; (2) flies raised at lower temperatures did not always outperform those developed at other temperatures; (3) there were no harmful cumulative effects after exposing both juveniles and adults to higher temperatures; (4) both latitudinal populations showed similar thermal plasticity patterns. The negative effect of high developmental temperature on reproductive performance, regardless of adult temperature, highlights the developmental stage as very critical and most vulnerable to climate change and associated heat waves.info:eu-repo/semantics/publishedVersio

No evidence for short‐term evolutionary response to a warming environment in Drosophila

Adaptive evolution is key in mediating responses to global warming and may sometimes be the only solution for species to survive.Such evolution will expectedly lead to changes in the populations’ thermal reaction norm and improve their ability to cope with stressful conditions. Conversely, evolutionary constraints might limit the adaptive response. Here, we test these expectations by performing a real-time evolution experiment in historically differentiated Drosophila subobscura populations. We address the phenotypic change after nine generations of evolution in a daily fluctuating environment with average constant temperature, or in a warming environment with increasing average and amplitude temperature across generations. Our results showed that (1) evolution under a global warming scenario does not lead to a noticeable change in the thermal response; (2) historical background appears to be affecting responses under the warming environment, particularly at higher temperatures; and (3) thermal reaction norms are trait dependent: although lifelong exposure to low temperature decreases fecundity and productivity but not viability,high temperature causes negative transgenerational effects on productivity and viability, even with high fecundity. These findings in such an emblematic organism for thermal adaptation studies raise concerns about the short-term effciency of adaptive responses to the current rising temperatures.info:eu-repo/semantics/acceptedVersio

Past history shapes evolution of reproductive success in a global warming scenario

Adaptive evolution is critical for animal populations to thrive in the fast-changing natural environments. Ectotherms are particularly vulnerable to global warming and, although their limited coping ability has been suggested, few real-time evolution experiments have directly accessed their evolutionary potential. Here, we report a long-term experimental evolution study addressing the evolution of Drosophila thermal reaction norms, after ∼30 generations under different dynamic thermal regimes: fluctuating (daily variation between 15 and 21 °C) or warming (daily fluctuation with increases in both thermal mean and variance across generations). We analyzed the evolutionary dynamics of Drosophila subobscura populations as a function of the thermally variable environments in which they evolved and their distinct background. Our results showed clear differences between the historically differentiated populations: high latitude D. subobscura populations responded to selection, improving their reproductive success at higher temperatures whereas their low latitude counterparts did not. This suggests population variation in the amount of genetic variation available for thermal adaptation, an aspect that needs to be considered to allow for better predictions of future climate change responses. Our results highlight the complex nature of thermal responses in face of environmental heterogeneity and emphasize the importance of considering inter-population variation in thermal evolution studies.info:eu-repo/semantics/acceptedVersio

Heat-induced female biased sex ratio during development is not mitigated after prolonged thermal selection

Abstract Background The negative impacts of climate change on biodiversity are consistently increasing. Developmental stages are particularly sensitive in many ectotherms. Moreover, sex-specific differences in how organisms cope with thermal stress can produce biased sex ratios upon emergence, with potentially major impacts on population persistence. This is an issue that needs investigation, particularly testing whether thermal selection can alleviate sex ratio distortions in the long-term is a critical but neglected issue. Here, we report an experiment analyzing the sex ratio patterns at different developmental temperatures in Drosophila subobscura populations subjected to long-term experimental evolution (~ 30 generations) under a warming environment. Results We show that exposure to high developmental temperatures consistently promotes sex ratio imbalance upon emergence, with a higher number of female than male offspring. Furthermore, we found that thermal selection resulting from evolution in a warming environment did not alleviate such sex ratio distortions generated by heat stress. Conclusions We demonstrate that heat stress during development can lead to clear sex ratio deviations upon emergence likely because of differential survival between sexes. In face of these findings, it is likely that sex ratio deviations of this sort occur in natural populations when facing environmental perturbation. The inability of many insects to avoid thermal shifts during their (more) sessile developmental stages makes this finding particularly troublesome for population subsistence in face of climate warming events

Differential exposure to second-generation anticoagulant rodenticides in raptors from continental and insular regions of the Iberian Peninsula

Beca Doctoral PIFULPGC-2020-CCSALUD-1 para Beatriz Martín Cruz Beca Post-Doctoral para Cristian Rial-Berriel (APCR2022010002) y Andrea Acosta-Dacal (APCR2022010003) Beca Doctoral PD/BD/150550/2019 para Ana Carromeu-Santos UIDP/50017/2020+UIDB/50017/2020+LA/P/0094/2020 Sofia I. GabrielThe global impact of anticoagulant rodenticides (ARs) on non-target species is well-recognized. Birds of prey, as apex predators, are highly vulnerable to AR exposure and are widely used as biomonitors for priority pollutants in Europe. This study investigates differential SGAR exposure in raptors from insular versus continental regions, hypothesizing greater exposure in insular areas due to ecological factors like reduced prey diversity, intensive rodenticide use, and resistant rodent populations. We analyzed the livers of 190 common kestrels (Falco tinnunculus) and 104 common buzzards (Buteo buteo) across the Iberian Peninsula and its archipelagos using LC-MS/MS to assess their role as AR sentinels and the differences between insular and continental areas. Results revealed a high prevalence (>80%) of second-generation anticoagulant rodenticides (SGARs), with brodifacoum and bromadiolone, being the most frequent. Multiple SGAR detections were also common (≈50%). A binomial logistic regression showed that species and region significantly influence the likelihood of SGAR exposure. Kestrels had a greater probability of exceeding 100 ng/g wet weight (ww) compared to buzzards. Raptors from insular territories were ten times more likely to have higher SGAR concentrations than those from continental areas. However, the legal restriction on SGAR bait concentrations that came into effect in 2018 did not significantly impact exposure levels. This study highlights the need for targeted conservation efforts to mitigate AR exposure risk in vulnerable island ecosystems.Universidad de Las Palmas de Gran CanariaGobierno de CanariasFundação para a Ciência e a Tecnologia (Portugal)Sección Deptal. de Farmacología y Toxicología (Veterinaria)Fac. de VeterinariaTRUEpu