The different sources of variation in inbreeding depression, heterosis and outbreeding depression in a metapopulation of Physa acuta

Abstract

Understanding how parental distance affects offspring fitness, i.e., the effects of inbreeding and outbreeding in natural populations, is a major goal in evolutionary biology. While inbreeding is often associated with fitness reduction (inbreeding depression), interpopulation outcrossing may have either positive (heterosis) or negative (outbreeding depression) effects. Within a metapopulation, all phenomena may occur with various intensities depending on the focal population (especially its effective size) and the trait studied. However, little is known about interpopulation variation at this scale. We here examine variation in inbreeding depression, heterosis, and outbreeding depression on life-history traits across a full-life cycle, within a metapopulation of the hermaphroditic snail Physa acuta. We show that all three phenomena can co-occur at this scale, although they are not always expressed on the same traits. A large variation in inbreeding depression, heterosis, and outbreeding depression is observed among local populations. We provide evidence that, as expected from theory, small and isolated populations enjoy higher heterosis upon outcrossing than do large, open populations. These results emphasize the need for an integrated theory accounting for the effects of both deleterious mutations and genetic incompatibilities within metapopulations and to take into account the variability of the focal population to understand the genetic consequences of inbreeding and outbreeding at this scale.

Figure 1.—

Crossing scheme for interpopulation hybridizations. Each population was crossed with at least one river and one pond population. Arrows are from females to males. Thirty-three types of interpopulation crosses were performed (note that the female Mos × male Lez cross could not be performed).

Figure 2.—

Inbreeding depression and heterosis for life-history traits. Left y-axes, the log-inbreeding depression (ln ID in A), and the log heterosis (ln H in B); right y-axes, classic inbreeding depression (A) and heterosis (B). Shaded bars, mean values over the two habitat types; open bars, means for ponds; and solid bars, means for rivers. Error bars were calculated as SEM over populations. RLS, reproductive life span; RLE, reproductive life expectancy; Fec., fecundity; LTRS, lifetime reproductive success; L₂₂, size at 22 days; L₁₅₀, size at 150 days. Note that ln ID and ln H (left y-axes) do not represent a simple logarithmic transformation of values presented in the right y-axes (see materials and methods for details).

Figure 3.—

Log-fitness traits for self-fertilized offspring (ln selfing, left) and interpopulation hybrids (ln inter, right) as a function of log-fitness traits for intrapopulation outcrossed offspring (ln intra). Only the most important fitness components are represented. (A) 0- to 15-day survival; (B) reproductive life span (RLS); (C) fecundity; (D) lifetime reproductive success (LTRS). Lines represent constant values of log-inbreeding depression (ln δ, left and log heterosis (ln H, right). Open squares, ponds; solid squares, rivers. Open areas represent positive values and shaded areas negative values of inbreeding depression and heterosis, respectively (note that negative heterosis represents outbreeding depression). Note change in scales among graphs.

Figure 4.—

Intra- and interpopulation outcrossing performances for the most important fitness components. (A) 0- to 15-day survival; (B) reproductive life span; (C) fecundity. Solid squares and lines represent intrapopulation outcrossing; shaded squares and lines represent interpopulation outcrossing. Results are presented for each pair of populations (two shaded squares and two solid squares). For instance, the first two populations on the left (Lam and Mos) should be read as follows: the solid square on the left represents the value for the Lam × Lam cross, and the shaded square represents the value for the cross female Lam × male Mos. The solid square on the right represents the value for the Mos × Mos cross, and the shaded square the value for the female Mos × male Lam cross. In this representation, differences between parental populations are indicated by the slope of the solid line, and asymmetries between reciprocal crosses are indicated by the slope of the shaded line. Different shadings denote heterosis (interpopulation hybrids fitter than intrapopulation crosses) and outbreeding depression (vice versa) as indicated. By convention, the river is on the left and the pond on the right in all mixed pairs of populations. Note that one cross (female Mos × male Lez) could not be performed.