Research Article: Does Haplodiploidy Purge Inbreeding Depression in Rotifer Populations?

Date Published: December 7, 2009

Publisher: Public Library of Science

Author(s): Ana M. Tortajada, María José Carmona, Manuel Serra, Stewart Plaistow.

Abstract: Inbreeding depression is an important evolutionary factor, particularly when new habitats are colonized by few individuals. Then, inbreeding depression by drift could favour the establishment of later immigrants because their hybrid offspring would enjoy higher fitness. Rotifers are the only major zooplanktonic group where information on inbreeding depression is still critically scarce, despite the fact that in cyclical parthenogenetic rotifers males are haploid and could purge deleterious recessive alleles, thereby decreasing inbreeding depression.

Partial Text: Inbreeding depression, or the decrease in fitness due to mating between relatives, is an important ecological and evolutionary phenomenon, which has been widely studied from multiple perspectives, such as population genetics, mating system evolution or conservation biology, and for a broad range or organisms [1], [2]. When a population is founded by a few individuals, inbreeding depression by drift may occur. The relationship between inbreeding depression and gene flow has emerged as a relevant topic to explore in the case of planktonic invertebrates inhabiting lakes and ponds (mainly cladocerans and rotifers), due to the population genetic structure detected for these organisms through molecular studies. Planktonic invertebrates are thought to have high passive dispersal abilities via resting stages [3]–[6]. However, strong differentiation in neutral genetic markers and in ecologically relevant traits has been reported [7]–[10], which suggests low levels of gene flow. De Meester et al.[11], extending the founding effects hypothesis of Boileau et al. [12], proposed the Monopolization Hypothesis to explain this paradox. According to this hypothesis, founding effects would persist due to (1) dilution, after population founding, of new immigrants in a large number of residents and (2) selection against immigrants arriving in a locally adapted population. Fast population growth from a few founders, persistent large population sizes, reinforced by large abundance of diapausing stages, and rapid local adaptation would make possible these effects.

Parental fertilization proportions did not show a pattern of inbreeding avoidance. Although P-clone combinations had a significant interaction effect on the parental fertilization proportion, the most negative P-clone interaction coefficients did not tend to occur in selfed crosses (Fig. 2, PFP). Moreover, the global parental fertilization proportion was similar for selfed and outcrossed crosses in both TOS (Poza Sur, the smallest population; see Methods for details) and HOS (Hondo Sur) populations (Fig. 3). Similarly, evidence for inbreeding depression on the proportion of diapausing egg-producing clones was not found in any of both populations. P-clone combinations had a significant interaction effect in TOS, but selfed crosses did not showed a clear tendency to have low interaction coefficients (Fig. 2, DEPC). Moreover, in both populations a global effect of the type of cross was not observed (selfed vs. outcrossed; Fig. 3). Nevertheless, in TOS a non-significant tendency to decrease the proportion of diapausing egg-producing clones was observed in selfed crosses (Fig. 2 and 3).

The results of this study show that inbreeding depression affects several fitness components of B. plicatilis life cycle. There is clear evidence that inbreeding negatively affects fitness components associated with the asexual phase. Inbreeding depression has been found in both populations studied for the proportion of F1 diapausing eggs yielding viable clones (i.e., the F1 egg hatching proportion times the F1 clone viability), and the growth rate of the F1 clones. These findings are consistent with the negative inbreeding effects pointed out in previous studies on rotifers [24], [25]. In contrast to our findings for the asexual phase, our results for the sexual phase are less clear. Evidence for inbreeding depression in the production of males exists for both TOS and HOS populations, as shown by parameters related to male production, even when the effect of culture density on this production was discounted. Nevertheless, an inbreeding effect on the proportion of clones able to produce diapausing eggs through selfing was not found in both TOS and HOS. Lack of evidence for inbreeding depression in the proportion of clones able to produce diapausing eggs might be the result of low statistical power, since sample size decreases with the successive life-cycle steps analyzed. Alternatively, most of the deleterious effects could be expressed in the embryo developmental process of the diapausing eggs and in the parthenogenetic proliferation of the first generations, because these phases involve many gene functions. Thus, our demonstration of inbreeding depression represents the first thorough study measuring fitness step by step throughout the life cycle in the phylum Rotifera.



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