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  • The dynamics of casual groups can keep free-riders at bay
    Publication . Fontanari, José F.; Santos, Mauro
    Understanding the conditions for maintaining cooperation in groups of unrelated individuals despite the presence of non-cooperative members is a major research topic in contemporary biological, sociological, and economic theory. The $N$-person snowdrift game models the type of social dilemma where cooperative actions are costly, but there is a reward for performing them. We study this game in a scenario where players move between play groups following the casual group dynamics, where groups grow by recruiting isolates and shrink by losing individuals who then become isolates. This describes the size distribution of spontaneous human groups and also the formation of sleeping groups in monkeys. We consider three scenarios according to the probability of isolates joining a group. We find that for appropriate choices of the cost-benefit ratio of cooperation and the aggregation-disaggregation ratio in the formation of casual groups, free-riders can be completely eliminated from the population. If individuals are more attracted to large groups, we find that cooperators persist in the population even when the mean group size diverges. We also point out the remarkable similarity between the replicator equation approach to public goods games and the trait group formulation of structured demes.
  • From Bayes to Darwin: Evolutionary search as an exaptation from sampling-based Bayesian inference
    Publication . Csillag, Márton; Giaffar, Hamza; Szathmáry, Eörs; Santos, Mauro; Czégel, Dániel
    Building on the algorithmic equivalence between finite population replicator dynamics and particle filtering based approximation of Bayesian inference, we design a computational model to demonstrate the emergence of Darwinian evolution over representational units when collectives of units are selected to infer statistics of high-dimensional combinatorial environments. The non-Darwinian starting point is two units undergoing a few cycles of noisy, selection-dependent information transmission, corresponding to a serial (one comparison per cycle), non-cumulative process without heredity. Selection for accurate Bayesian inference at the collective level induces an adaptive path to the emergence of Darwinian evolution within the collectives, capable of maintaining and iteratively improving upon complex combinatorial information. When collectives are themselves Darwinian, this mechanism amounts to a top-down (filial) transition in individuality. We suggest that such a selection mechanism can explain the hypothesized emergence of fast timescale Darwinian dynamics over a population of neural representations within animal and human brains, endowing them with combinatorial planning capabilities. Further possible physical implementations include prebiotic collectives of non-replicating molecules and reinforcement learning agents with parallel policy search.
  • Mate-choice copying accelerates species range expansion
    Publication . Sapage, Manuel; Santos, Mauro; Matos, Margarida; Schlupp, Ingo; Varela, Susana A. M.
    Mate-choice copying is a type of social learning in which females can change their mate preference after observing the choice of others. This behaviour can potentially affect population evolution and ecology, namely through increased dispersal and reduced local adaptation. Here, we simulated the effects of mate-choice copying in populations expanding across an environmental gradient to understand whether it can accelerate or retard the expansion process. Two mate-choice copying strategies were used: (i) when females target a single individual and (ii) when females target similar individuals. We also simulated cases where the male trait singled out by females with mate choice maps perfectly onto his genotype or is influenced by genotype-by-environment interactions. These rules have different effects on the results. When a trait is determined by genotype alone, populations where copier females target all similar males expand faster and the number of potential copiers increased. However, when preference is determined by genotype-by-environment interactions, populations where copier females target a single male had higher dispersal and also expand faster, but the potential number of copiers decreases. The results show that mate-choice copying can accelerate the expansion process, although its adaptiveness depends on the information animals use in different contexts.
  • No evidence for short‐term evolutionary response to a warming environment in Drosophila
    Publication . Santos, Marta A.; Carromeu‐Santos, Ana; Quina, Ana; Santos, Mauro; Matos, Margarida; Simões, Pedro
    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.
  • Heat-induced female biased sex ratio during development is not mitigated after prolonged thermal selection
    Publication . Santos, Marta A.; Antunes, Marta; Grandela, Afonso; Carromeu-Santos, Ana; Quina, Ana; Santos, Mauro; Matos, Margarida; Simões, Pedro
    Background The negative impacts of climate change on biodiversity are consistently increasing. Developmen‑ tal stages are particularly sensitive in many ectotherms. Moreover, sex-specifc diferences 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 diferent 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 ofspring. Furthermore, we found that thermal selec‑ tion 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 diferential survival between sexes. In face of these fndings, 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.
  • Directional selection coupled with kin selection favors the establishment of senescence
    Publication . Szilágyi, András; Czárán, Tamás; Santos, Mauro; Szathmáry, Eörs
    Background Conventional wisdom in evolutionary theory considers aging as a non-selected byproduct of natural selection. Based on this, conviction aging was regarded as an inevitable phenomenon. It was also thought that in the wild organisms tend to die from diseases, predation and other accidents before they could reach the time when senescence takes its course. Evidence has accumulated, however, that aging is not inevitable and there are organisms that show negative aging even. Furthermore, old age does play a role in the deaths of many different organisms in the wild also. The hypothesis of programmed aging posits that a limited lifespan can evolve as an adaptation (i.e., positively selected for) in its own right, partly because it can enhance evolvability by eliminating “outdated” genotypes. A major shortcoming of this idea is that non-aging sexual individuals that fail to pay the demographic cost of aging would be able to steal good genes by recombination from aging ones. Results Here, we show by a spatially explicit, individual-based simulation model that aging can positively be selected for if a sufficient degree of kin selection complements directional selection. Under such conditions, senescence enhances evolvability because the rate of aging and the rate of recombination play complementary roles. The selected aging rate is highest at zero recombination (clonal reproduction). In our model, increasing extrinsic mortality favors evolved aging by making up free space, thereby decreasing competition and increasing drift, even when selection is stabilizing and the level of aging is set by mutation-selection balance. Importantly, higher extrinsic mortality is not a substitute for evolved aging under directional selection either. Reduction of relatedness decreases the evolved level of aging; chance relatedness favors non-aging genotypes. The applicability of our results depends on empirical values of directional and kin selection in the wild. Conclusions We found that aging can positively be selected for in a spatially explicit population model when sufficiently strong directional and kin selection prevail, even if reproduction is sexual. The view that there is a conceptual link between giving up clonal reproduction and evolving an aging genotype is supported by computational results.
  • Experimental Evolution in a Warming World: The Omics Era
    Publication . Santos, Marta A.; Carromeu-Santos, Ana; Quina, Ana S; Antunes, Marta; Kristensen, Torsten N; Santos, Mauro; Matos, Margarida; De mendonça fragata almeida, Inês; Simões, Pedro
    A comprehensive understanding of the genetic mechanisms that shape species responses to thermal variation is essential for more accurate predictions of the impacts of climate change on biodiversity. Experimental evolution with high-throughput resequencing approaches (evolve and resequence) is a highly effective tool that has been increasingly employed to elucidate the genetic basis of adaptation. The number of thermal evolve and resequence studies is rising, yet there is a dearth of efforts to integrate this new wealth of knowledge. Here, we review this literature showing how these studies have contributed to increase our understanding on the genetic basis of thermal adaptation. We identify two major trends: highly polygenic basis of thermal adaptation and general lack of consistency in candidate targets of selection between studies. These findings indicate that the adaptive responses to specific environments are rather independent. A review of the literature reveals several gaps in the existing research. Firstly, there is a paucity of studies done with organisms of diverse taxa. Secondly, there is a need to apply more dynamic and ecologically relevant thermal environments. Thirdly, there is a lack of studies that integrate genomic changes with changes in life history and behavioral traits. Addressing these issues would allow a more in-depth understanding of the relationship between genotype and phenotype. We highlight key methodological aspects that can address some of the limitations and omissions identified. These include the need for greater standardization of methodologies and the utilization of new technologies focusing on the integration of genomic and phenotypic variation in the context of thermal adaptation.