Variation in inbreeding depression within and among Caenorhabditis species

Abstract

Outbreeding populations harbor large numbers of recessive deleterious alleles that reduce the fitness of inbred individuals, and this inbreeding depression potentially shapes the evolution of mating systems, acting as a counterweight to the inherent selective advantage of self-fertilization. The population biological factors that influence inbreeding depression are numerous and often difficult to disentangle. We investigated the utility of obligately-outcrossing (gonochoristic) Caenorhabditis nematodes as models for inbreeding depression. By systematically inbreeding lines from ten populations and tracking line extinction, we found that inbreeding depression is universal but highly variable among species and populations. Inbreeding depression was detected across the life cycle, from mating to embryo production to embryonic viability and larval growth, and reciprocal crosses implicated female-biased effects. In most cases, the surviving inbred lines have dramatically reduced fitness, but the variance among inbred lines is substantial and compatible with the idea that inbreeding depression need not be an obstacle to the evolution of selfing in these worms. Populations of some species, including Caenorhabditis becei, exhibited modest inbreeding depression and could be tractable laboratory models for gonochoristic Caenorhabditis.

Keywords: Caenorhabditis; Selfing; inbreeding depression; mating-system transitions; recessive genetic variation.

Figure 1.

A. During the course of 20 generations of serial full-sib mating, the majority of lines for each of 11 Caenorhabditis isolates went extinct. The two lines for each color represent the two different founding isolates for each wild population. B. In the absence of inbreeding depression, the expected survival curves follow exponential decay with rate –e^A, reflecting a constant probability of cross failure. The difference between panels A and B demonstrates the extent of concealed genetic load (B_R), which is significant for every strain except the control strain, C. elegans fog-2. This strain began the experiment fully inbred, and its steep die-off reflects its high but constant rate of cross failure. See Table 1 for estimates, errors, and p-values.

Figure 2.

Inbred lines have reduced and heterogeneous fitness relative to their ancestor. The y-axis shows the relative fitness of the five ancestors and several of their inbred descendants. Each ancestor’s mean relative fitness (filled circles) is set to 1. Each point is a single mated female, and the circles represent strain means.

Figure 3.

Crosses between related inbred lines of C. panamensis show complementation and maternal effects. The y-axis shows the log of the number of hours required for a population founded by two males and two females to exhaust a fixed quantity of resources; the population at that point typically includes thousands of grandchildren of the founders. Points lower on the y-axis represent populations with faster population growth and consequently greater fitness. Each point is a population and gray circles indicate means. The F₁s are the product of matings between females of strain A and males of strain B (F₁^AB) or the reciprocal cross (F₁^BA).