Evolutionary Genetics
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The main objective of the Evolutionary Genetics group is to study the genetics of adaptation using experimental evolution, by testing current evolutionary theory. Adaptation and the study of natural selection and its consequences are central to any understanding of biology because they provide a comprehensive framework for the origin, divergence and maintenance of diversity. We use experimental evolution to integrate the study of variation at the phenotype level with the study of variation at the genotype level. Since setting up at the IGC, we have established experimental evolution populations of Caenorhabditis elegans, whose ecology is described by discrete non-overlapping generations at constant 104 census sizes, under benign resource conditions. These populations were manipulated to initially have levels of outcrossing and genetic diversity. Phenotyping is carried out at the level of fitness-proxies, life-history and RNA expression. Genome-wide linkage disequilibrium association mapping is carried out to determine the number and relative effects of the loci underlying adaptation. Numerical simulations are used to obtain the expected distributions of relevant statistics under the conditions of experimental evolution.
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- Quantitative genetics of functional characters in Drosophila melanogaster populations subjected to laboratory selectionPublication . Teotónio, H; Matos, M; Rose, MRWhat are the genetics of phenotypes other than fitness, in outbred populations? To answer this question. the quantitative-genetic basis of divergence was characterized for outbred Drosophila melanogaster populations that had previously undergone selection to enhance characters related to fitness. Line-cross analysis using first-generation and second-generation hybrids from reciprocal crosses was conducted for two types of cross, each replicated fivefold. One type of cross was between representatives of the ancestral population, a set of five populations maintained for several hundred generations on a two-week discrete-generation life cycle and a set of five populations adapted to starvation stress. The other type of cross was between the same set of ancestral-representative populations and another set of five populations selected for accelerated development from egg to egg. Developmental time from coo to eclosion. starvation resistance, dry body weight and fecundity at day 14 from ego were fit to regression models estimating single-locus additive and dominant effects, maternal and paternal effects. and digenic additive and dominance epistatic effects. Additive genetic variation explained most of the differences between populations, with additive maternal and cytoplasmic effects also commonly found. Both within-locus and between-locus dominance effects were inferred in some cases, as well as one instance of additive epistasis. Some of these effects may have been caused by linkage disequilibrium. We conclude with a brief discussion concerning the relationship of the genetics of population differentiation to adaptation.
- Genetic variation for outcrossing among Caenorhabditis elegans isolatesPublication . Teotónio, H; Manoel, D; Phillips, PCThe evolution of breeding systems results from the existence of genetic variation and selective forces favoring different outcrossing rates. In this study we determine the extent of genetic variation for characters directly related to outcrossing, such as male frequency, male mating ability, and male reproductive success, in several wild isolates of the nematode Caenorhabditis elegans. This species is characterized by an androdioecious breeding system in which males occur with hermaphrodites that can either self-fertilize or outcross with males. We find genetic variation for all characters measured, but also find that environmental variation is a large fraction of the total phenotypic variance. We further determine the existence of substantial genetic variation for population competitive performance in several laboratory environments. However, these measures are uncorrelated with outcrossing characters. The data presented here contribute to an understanding of male maintenance in natural populations through their role in outcrossing.
- Selection against males in Caenorhabditis elegans under two mutational treatmentsPublication . Manoel, D; Carvalho, S; Phillips, PC; Teotónio, HWithin populations with mixed mating systems, selfing is expected to be favoured over outcrossing unless a countervailing process such as severe inbreeding depression is present. In this study, we consider the relationship between the expression of deleterious alleles and the maintenance of outcrossing in the nematode species, Caenorhabditis elegans. This species is characterized by an androdioecious breeding system composed of males at low frequency and self-fertilizing hermaphrodites that can only outcross via males. Here, we find that experimentally increasing the mutational load in four different isogenic wild isolates using 10 generations of Ethylmethane sulphonate (EMS) and UV irradiation mutagenesis significantly diminishes the cost of males. Males are maintained at higher frequencies in mutagenized versus non-mutagenized populations. Nevertheless, males still tend to be driven to low frequencies within isolates that are known to be prone to lose males. Further, we determine the viability effects of a single round of mutagen exposure and find that, for EMS, outcrossing overcomes the almost completely recessive and nearly lethal effects generated. We briefly interpret our results in light of current evolutionary theory of outcrossing rates.
- Experimental evolution reveals natural selection on standing genetic variationPublication . Teotónio, H; Chelo, IM; Bradic, M; Rose, MR; Long, ADEvolution depends on genetic variation generated by mutation or recombination from standing genetic variation. In sexual organisms, little is known about the molecular population genetics of adaptation and reverse evolution(1-11). We carry out 50 generations of experimental reverse evolution in populations of Drosophila melanogaster, previously differentiated by forward evolution, and follow changes in the frequency of SNPs in both arms of the third chromosome. We characterize the effects of sampling finite population sizes and natural selection at the genotype level. We demonstrate that selection has occurred at several loci and further that there is no general loss or gain of allele diversity. We also observe that despite the complete convergence to ancestral levels of adaptation, allele frequencies only show partial return.
- Evolution of Outcrossing in Experimental Populations of Caenorhabditis elegansPublication . Teotonio, Henrique; Carvalho, Sara; Manoel, Diogo; Roque, Miguel; Chelo, Ivo M.Caenorhabditis elegans can reproduce exclusively by self-fertilization. Yet, males can be maintained in laboratory populations, a phenomenon that continues to puzzle biologists. In this study we evaluated the role of males in facilitating adaptation to novel environments. For this, we contrasted the evolution of a fitness component exclusive to outcrossing in experimental populations of different mating systems. We introgressed a modifier of outcrossing into a hybrid population derived from several wild isolates to transform the wild-type androdioecious mating system into a dioecious mating system. By genotyping 375 single-nucleotide polymorphisms we show that the two populations had similar standing genetic diversity available for adaptation, despite the occurrence of selection during their derivation. We then performed replicated experimental evolution under the two mating systems from starting conditions of either high or low levels of diversity, under defined environmental conditions of discrete non-overlapping generations, constant density at high population sizes (N = 10(4)), no obvious spatial structure and abundant food resources. During 100 generations measurements of sex ratios and male competitive performance showed: 1) adaptation to the novel environment; 2) directional selection on male frequency under androdioecy; 3) optimal outcrossing rates of 0.5 under androdioecy; 4) the existence of initial inbreeding depression; and finally 5) that the strength of directional selection on male competitive performance does not depend on male frequencies. Taken together, these results suggest that androdioecious males are maintained at intermediate frequencies because outcrossing is adaptive.
- THE OPPORTUNITY FOR BALANCING SELECTION IN EXPERIMENTAL POPULATIONS OFCAENORHABDITIS ELEGANSPublication . Chelo, Ivo M.; Teotónio, HenriqueThe role of balancing selection in maintaining diversity during the evolution of sexual populations to novel environments is poorly understood. To address this issue, we studied the impact of two mating systems, androdioecy and dioecy, on genotype distributions during the experimental evolution of Caenorhabditis elegans. We analyzed the temporal trajectories of 334 single nucleotide polymorphisms, covering 1/3 of the genome, and found extensive allele frequency changes and little loss of heterozygosities after 100 generations. As modeled with numerical simulations, SNP differentiation was consistent with genetic drift and average fitness effects of 2%, assuming that selection acted independently at each locus. Remarkably, inbreeding by self-fertilization was of little consequence to SNP differentiation. Modeling selection on deleterious recessive alleles suggests that the initial evolutionary dynamics can be explained by associative overdominance, but not the later stages because much lower heterozygosities would be maintained during experimental evolution. By contrast, models with selection on true overdominant loci can explain the heterozygote excess observed at all periods, particularly when negative epistasis or independent fitness effects were considered. Overall, these findings indicate that selection at single loci, including purging of recessive alleles, underlies most of the genetic differentiation accomplished during the experiment. Nonetheless, they also imply that maintenance of genetic diversity may in large part be due to balancing selection at multiple loci.
- An experimental test on the probability of extinction of new genetic variantsPublication . Chelo, Ivo M.; Nédli, Judit; Gordo, Isabel; Teotónio, HenriqueIn 1927, J.B.S. Haldane reasoned that the probability of fixation of new beneficial alleles is twice their fitness effect. This result, later generalized by M. Kimura, has since become the cornerstone of modern population genetics. There is no experimental test of Haldane's insight that new beneficial alleles are lost with high probability. Here we demonstrate that extinction rates decrease with increasing initial numbers of beneficial alleles, as expected, by performing invasion experiments with inbred lines of the nematode Caenorhabditis elegans. We further show that the extinction rates of deleterious alleles are higher than those of beneficial alleles, also as expected. Interestingly, we also find that for these inbred lines, when at intermediate frequencies, the fate of invaders might not result in their ultimate fixation or loss but on their maintenance. Our study confirms the key results from classical population genetics and highlights that the nature of adaptation can be complex.
- The role of hermaphrodites in the experimental evolution of increased outcrossing rates in Caenorhabditis elegansPublication . Carvalho, Sara; Chelo, Ivo M; Goy, Christine; Teotónio, HenriqueWhy most organisms reproduce via outcrossing rather than selfing is a central question in evolutionary biology. It has long ago been suggested that outcrossing is favoured when it facilitates adaptation to novel environments. We have previously shown that the experimental evolution of increased outcrossing rates in populations of the male-hermaphrodite nematode Caenorhabditis elegans were correlated with the experimental evolution of increased male fitness. However, it is unknown whether outcrossing led to adaptation, and if so, which fitness components can explain the observed increase in outcrossing rates.
- Hermaphrodite life history and the maintenance of partial selfing in experimental populations of Caenorhabditis elegansPublication . Carvalho, Sara; Phillips, Patrick C; Teotónio, HenriqueClassic population genetics theory predicts that mixed reproductive systems, where self reproduction (selfing) and outcrossing co-exist, should not be as common as they are in nature. One means of reconciling theory with observations is to recognize that sexual conflict between males and hermaphrodites and/or constraints in the allocation of resources towards sex functions in hermaphrodites can balance the fitness components of selfing and outcrossing.
- Reproductive assurance drives transitions to self-fertilization in experimental Caenorhabditis elegansPublication . Theologidis, Ioannis; Chelo, Ivo M; Goy, Christine; Teotónio, HenriqueEvolutionary transitions from outcrossing between individuals to selfing are partly responsible for the great diversity of animal and plant reproduction systems. The hypothesis of 'reproductive assurance' suggests that transitions to selfing occur because selfers that are able to reproduce on their own ensure the persistence of populations in environments where mates or pollination agents are unavailable. Here we test this hypothesis by performing experimental evolution in Caenorhabditis elegans.