Eco-evolutionary genetics
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It is well known that interactions between organisms play an important role in adaptation to new environments. This occurs specially in situations where negative feedbacks at the population level lead to the maintenance of polymorphisms by selection or when interactions between individuals of different species exert strong selective pressures, as in the case of predator-prey or host-parasite relationships. Understanding how these complex interactions shape adaptation to new environments requires knowledge about how evolution affects ecological relationships, preferentially in a multilevel approach that ranges from genes to ecosystems. I am interested in addressing these questions experimentally, using the nematode Caenorhabditis elegans and the bacterium Escherichia coli. Under well-defined laboratory conditions, in co-culture or isolation, these two biological models will help understand: 1) how interactions between organisms influence adaptation; and, 2) what is the molecular basis of these complex dynamics. Ultimately, the goal will be to understand if what we know about the genetics of adaptation needs to be rethought in light of an evolving ecology.
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- 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.
- 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.
- Experimental determination of invasive fitness in Caenorhabditis elegansPublication . Chelo, Ivo MEstimation of fitness is a key step in experimental evolution studies. However, no established methods currently exist to specifically estimate how successful new alleles are in invading populations. The main reason is that most assays do not accurately reflect the randomness associated with the first stages of the invasion, when invaders are rare and extinctions are frequent. In this protocol, I describe how such experiments can be done in an effective way. By using the nematode model, Caenorhabditis elegans, a large number of invasion experiments are set up, whereby invading individuals carrying a visual marker are introduced into populations in very low numbers. The number of invaders counted in consecutive generations, together with the number of extinctions, is then used in the context of individual-based computer simulations to provide likelihood (Lk) estimates for fitness. This protocol can take up to five generations of experimental invasions and a few hours of computer processing time.
- Polygenicity and Epistasis Underlie Fitness-Proximal Traits in the Caenorhabditis elegans Multiparental Experimental Evolution (CeMEE) PanelPublication . Noble, Luke M; Chelo, Ivo; Guzella, Thiago; Afonso, Bruno; Riccardi, David D; Ammerman, Patrick; Dayarian, Adel; Carvalho, Sara; Crist, Anna; Pino-Querido, Ania; Shraiman, Boris; Rockman, Matthew V; Teotónio, HenriqueUnderstanding the genetic basis of complex traits remains a major challenge in biology. Polygenicity, phenotypic plasticity and epistasis contribute to phenotypic variance in ways that are rarely clear. This uncertainty can be problematic for estimating heritability, for predicting individual phenotypes from genomic data, and for parameterizing models of phenotypic evolution. Here we report an advanced recombinant inbred line (RIL) quantitative trait locus (QTL) mapping panel for the hermaphroditic nematode Caenorhabditis elegans, the C. elegans multiparental experimental evolution (CeMEE) panel. The CeMEE panel, comprising 507 RILs at present, was created by hybridization of 16 wild isolates, experimental evolution for 140-190 generations, and inbreeding by selfing for 13-16 generations. The panel contains 22% of single nucleotide polymorphisms known to segregate in natural populations, and complements existing C. elegans mapping resources by providing fine resolution and high nucleotide diversity across >95% of the genome. We apply it to study the genetic basis of two fitness components, fertility and hermaphrodite body size at time of reproduction, with high broad sense heritability in the CeMEE. While simulations show we should detect common alleles with additive effects as small as 5%, at gene-level resolution, the genetic architectures of these traits does not feature such alleles. We instead find that a significant fraction of trait variance, approaching 40% for fertility, can be explained by sign epistasis with main effects below the detection limit. In congruence, phenotype prediction from genomic similarity, while generally poor (r2 < 10%), requires modeling epistasis for optimal accuracy, with most variance attributed to the rapidly evolving chromosome arms.
- 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.
- 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.