Behavioral degradation under mutation accumulation in Caenorhabditis elegans

Abstract

Spontaneous mutations play a fundamental role in the maintenance of genetic variation in natural populations, the nature of inbreeding depression, the evolution of sexual reproduction, and the conservation of endangered species. Using long-term mutation-accumulation lines of the nematode Caenorhabditis elegans, we estimate the rate and magnitude of mutational effects for a suite of behaviors characterizing individual chemosensory responses to a repellant stimulus. In accordance with evidence that the vast majority of mutations are deleterious, we find that behavioral responses degrade over time as a result of spontaneous mutation accumulation. The rate of mutation for behavioral traits is roughly of the same order or slightly smaller than those previously estimated for reproductive traits and the average size of the mutational effects is also comparable. These results have important implications for the maintenance of genetic variation for behavior in natural populations as well as for expectations for behavioral change within endangered species and captive populations.

Figure 1.—

Computerized tracking of nematode behavior in response to a repellent chemical (linoleic acid, located at the star). Lines show the path taken by an individual nematode over a 4-min period, beginning at the circle and ending at the arrowhead. (A) An individual from the ancestral control line showing a clear avoidance response. (B) An individual from one of the mutation accumulation lines that showed low avoidance scores. Directness is given by the beeline distance divided by the total path length. Velocity and turn rate are estimated, respectively, using instantaneous changes in speed and angle as the individual navigates away from the chemical. Note the change in scale between the two graphs.

Figure 2.—

Change in behavior after 370 generations of mutation accumulation. Average values for the unmutated control (shaded bar), the mutation accumulation lines (solid bar), and the control in the absence of the repellent chemical (open bar) are given. Behavior strongly declines under the accumulation of spontaneous mutations, either becoming more similar to the control in the absence of a stimulus (directness and turn rate) or simply showing an overall degradation in response (velocity). Error bars are 95% C.I.

Figure 3.—

Change in variance among lines under mutation accumulation. Pseudoreplicate control lines (shaded bars) provide estimates of the among-line environmental variance. The increase in variance beyond that shown by the mutation accumulation lines (solid bars) provides estimates of the genomic mutation rate and the average size of mutational effects.