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, 109 (46), 18862-7

Allard's Argument Versus Baker's Contention for the Adaptive Significance of Selfing in a Hermaphroditic Fish

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Allard's Argument Versus Baker's Contention for the Adaptive Significance of Selfing in a Hermaphroditic Fish

John C Avise et al. Proc Natl Acad Sci U S A.

Abstract

Fertilization assurance (Baker's contention) and multilocus coadaptation (Allard's argument) are two distinct hypotheses for the adaptive significance of self-fertilization in hermaphroditic taxa, and both scenarios have been invoked to rationalize isogenicity via incest in various plants and invertebrate animals with predominant selfing. Here we contrast Allard's argument and Baker's contention as applied to the world's only known vertebrate that routinely self-fertilizes. We pay special attention to frequencies of locally most common multilocus genotypes in Floridian populations of the Mangrove Rivulus (Kryptolebias marmoratus). Isogenicity patterns in this fish appear inconsistent with Allard's argument, thus leaving Baker's contention as the more plausible scenario (a result also supported by natural history information for this species). These results contrast with the isogenicity patterns and conclusions previously drawn from several self-fertilizing plants and invertebrate animal species. Thus, the adaptive significance of selfing apparently varies across hermaphroditic taxa.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Expected declines in population formula image and shifts in the frequencies of isogenic genotypes across eight generations of selfing, starting from an outbred deme in generation 0. Multilocus genotypes that are effectively isogenic begin to emerge by generation 5; some of these may soon proliferate under the influence of natural selection (and/or genetic drift). For example, isogenic lineage EE (black-tailed fish) represents only 10% of the population in generation 5 but increases to 70% of the population by generation 8. Similarly, isogenotype BB (striped body) increases to 20% of the population by generation 8. The demise of any isogenic lineage (such as the termination of FF in generation 5 or the disappearance of CC in generation 6) can be interpreted to register either reproductive failure or an outcross event by the focal individual(s).
Fig. 2.
Fig. 2.
Theoretical evolutionary dynamics of heterozygosity (the black-dot curve, Left) and LMCMLG frequencies (the three curves, Right) in a population of self-fertilizing hermaphrodites. The shaded box indicates the broad range of positive adaptive values and generation times under which expected frequencies of the LMCMLG are expected to be rather high (i.e., >0.10) under Allard’s scenario.
Fig. 3.
Fig. 3.
Frequencies of the LMCMLG in populations of Kryptolebias marmoratus [n = 12 Floridian populations (refs. and 45), Arabidopsis thaliana [n = 39 (ref. 46)], Avena barbata [n = 50 (ref. 12)], and Rumina decollata [n = 4 [ref. 16)]. Only samples with 10 or more assayed individuals are included.
Fig. 4.
Fig. 4.
Proportionate representations of different multilocus genotypes in four representative local populations each of Kmar, Arabidopsis, Avena, and Rumina. White regions at the top of each bar register pooled singleton genotypes, which were common in Kmar but generally much less so in assayed populations of the other three self-fertilizing species.

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