Evolution of Outcrossing in Experimental Populations of Caenorhabditis elegans

Abstract

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 = 104), 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.

Adaptation costs to constant and alternating polluted environments

“…The population was kept in the experimental conditions described in Teotónio et al. (2012) for over 140 generations prior to our study, and about 30% of individuals were male.…”

“…Caenorhabditis elegans is an androdioecious organism (i.e., self‐fertilization of hermaphrodites and facultative outcross with males). We used a stock population of C. elegans , composed of a mixture of 16 wild isolates, so that we could obtain a study population with a large genetic diversity (Teotónio, Carvalho, Manoel, Roque, & Chelo, 2012). This composite population ensured that its genetic architecture did not result from past selection pressures caused by the presence of a pollutant.…”

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

“…It is also important to consider how standing genetic variation can affect outcrossing rate dynamics in the absence of parasites. Teotonio, Carvalho, Manoel, Roque, and Chelo (2012) created high‐ and low‐diversity replicates of a hybrid C. elegans population derived from several wild isolates and passaged them for 100 generations in a novel laboratory environment. Male frequency was stably maintained around 20% in high‐diversity populations, and male frequency increased from 0% to near 14% in low‐diversity populations.…”

“…Although the inbred populations in Teotonio et al. (2012) and the N2 populations in Stewart and Phillips (2002) can both be described as “low‐diversity” (Sivasundar & Hey, 2003), their origins and observed outcrossing rate dynamics were very different. Taken together, these results suggest that both the level and the nature of standing genetic variation in a population will affect outcrossing rate dynamics, depending on whether a population is experiencing inbreeding depression or outbreeding depression.…”

Experimental determination of invasive fitness in Caenorhabditis elegans

“…elegans was chosen to experimentally model the invasion dynamics of beneficial alleles in populations mainly because, by following standard maintenance procedures 10,11 , it can be made to conform to the simplest scenario of the Wright-Fisher model of allele frequency change, where all individuals reproduce at the same time (generations are discrete), the offspring replaces progenitors in the population (generations are non-overlapping), and populations sizes are high and constant 2 .…”