A threefold genetic allee effect: population size affects cross-compatibility, inbreeding depression and drift load in the self-incompatible Ranunculus reptans

Abstract

A decline in population size can lead to the loss of allelic variation, increased inbreeding, and the accumulation of genetic load through drift. We estimated the fitness consequences of these processes in offspring of controlled within-population crosses from 13 populations of the self-incompatible, clonal plant Ranunculus reptans. We used allozyme allelic richness as a proxy for long-term population size, which was positively correlated with current population size. Crosses between plants of smaller populations were less likely to be compatible. Inbreeding load, assessed as the slope of the relationship between offspring performance and parental kinship coefficients, was not related to population size, suggesting that deleterious mutations had not been purged from small populations. Offspring from smaller populations were on average more inbred, so inbreeding depression in clonal fitness was higher in small populations. We estimated variation in drift load from the mean fitness of outbred offspring and found enhanced drift load affecting female fertility within small populations. We conclude that self-incompatibility systems do not necessarily prevent small populations from suffering from inbreeding depression and drift load and may exacerbate the challenge of finding suitable mates.

Figure 1.—

Expected relationship between parental kinship coefficient and offspring fitness for populations of different size. Large populations have a high inbreeding load, because inbreeding and thus purging of deleterious mutations have rarely happened. Small populations with some history of inbreeding have already lost deleterious mutations of large effect due to inbreeding. Consequently, their inbreeding load is low. On the other hand, drift load is expected to be higher in small populations, and so their outbred offspring are relatively less fit in comparison to those of large populations.

Figure 2.—

Relationship between allelic diversity and (A) population means of clonal offspring fitness (untransformed data) and (B) inbreeding depression ID in clonal fitness after the exclusion of self-incompatible crosses (N = 13, values based on transformed data).

Figure 3.—

Relationship between allelic diversity and (A) population mean seed set (untransformed data) and (B) relative number of incompatible crosses (N = 13). The SI system leads to a reduced number of available mating partners in long-term small populations.

Figure 4.—

Relationship between allelic diversity and (A) population means in offspring seed production (untransformed data) and (B) drift load in offspring seed production after the exclusion of self-incompatible crosses (N = 13, means of untransformed data). Long-term small populations have a higher drift load.

Figure 5.—

Fitness estimates for sexual and clonal reproduction of R. reptans offspring (A and B) and four life-stage fitness components (C–F) regressed on kinship coefficient between the parents. Results from the 13 populations are represented by separate lines.

Figure 6.—

Mean parental kinship coefficient of all surviving individuals at six life stages of R. reptans. The six life stages are parents, ovules within crossed flowers, developed seeds, germinated seedlings, rooted rosettes, and seeds produced by the F₁ offspring. The 13 populations are represented by separate lines: dotted lines for long-term small populations (H_s: 0.386–0.410), dashed lines for medium-sized populations (H_s: 0.421–0.444), and solid lines for large populations (H_s: 0.471–0.498). (The first two classes of 7 populations include the 6 populations with the smallest size measured in the field.) Small populations had on average the highest kinship coefficients between randomly chosen parents, and, after crossing, the SI system and selection acted most strongly against inbred crosses, leading to a decrease of mean parental kinship coefficient in adult offspring.