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Allardts Argument Versus Bakerts Contention for the Adaptive Allard’s argument versus Baker’s contention for the adaptive significance of selfing in a hermaphroditic fish John C. Avise1 and Andrey Tatarenkov Department of Ecology and Evolutionary Biology, University of California, Irvine, CA 92697 Contributed by John C. Avise, October 2, 2012 (sent for review June 29, 2012) Fertilization assurance (Baker’s contention) and multilocus coadap- heterogeneity” and thus “natural selection was the predominant tation (Allard’s argument) are two distinct hypotheses for the integrating force in shaping the specific genetic structure of dif- adaptive significance of self-fertilization in hermaphroditic taxa, ferent local populations as well as the adaptive landscape.” With and both scenarios have been invoked to rationalize isogenicity regard to purported evolutionary benefits of self-fertilization as via incest in various plants and invertebrate animals with predom- a tactical component of a mixed-mating strategy, for shorthand we inant selfing. Here we contrast Allard’s argument and Baker’s con- will refer to this genomic-coadaptation scenario as Allard’s ar- tention as applied to the world’s only known vertebrate that gument for the adaptive significance of selfing. routinely self-fertilizes. We pay special attention to frequencies Soon thereafter, Robert Selander and colleagues published an of locally most common multilocus genotypes in Floridian popula- analogous series of studies documenting multilocus coadaptation tions of the Mangrove Rivulus (Kryptolebias marmoratus). Isoge- in local populations of terrestrial hermaphroditic snails with high nicity patterns in this fish appear inconsistent with Allard’s selfing rates (13–16). Again, specific multilocus suites of alleles argument, thus leaving Baker’s contention as the more plausible appeared to be coadapted to particular ecological conditions and scenario (a result also supported by natural history information for thereby often were driven to moderate or high frequencies in this species). These results contrast with the isogenicity patterns populations of these invertebrate animals. and conclusions previously drawn from several self-fertilizing Long before the works of Allard and Selander, however, Her- plants and invertebrate animal species. Thus, the adaptive signif- bert Baker (17, 18) had proposed a very different hypothesis for icance of selfing apparently varies across hermaphroditic taxa. the adaptive significance of self-fertilization, especially in the context of establishment after long distance dispersal (e.g., weeds, Baker’srule| coadapted genes | androdioecy | reproductive assuarance island colonization). According to Baker (19), fitness payoffs from selfing derive primarily from fertilization assurance [also known he mating system of many hermaphroditic plants and in- as “reproductive assurance” (20–22)] during island colonization Tvertebrate animals includes at least occasional self-fertiliza- or after long distance dispersal into distant habitats where con- tion (1–4). Why selfing is so common poses an evolutionary specifics might not be available for outbreeding. (This advantage enigma because self-fertilization is an extreme form of incest that also had been appreciated by Darwin.) Unlike obligate out- often reduces genetic fitness via inbreeding depression (5). Why crossers that lack the capacity to reproduce without a mate, each then do so many dual-sex organisms routinely self-fertilize? One self-compatible individual is reproductively self-sufficient. Baker standard explanation is that the transmission advantage of selfing interpreted fertilization assurance to be the key advantage of compared with outcrossing is sufficient to outweigh inbreeding selfing, an argument that gained empirical support from docu- depression and thus enable selfing to invade a population of mented associations—across plant species (23, 24), and particu- outcrossers (6). larly for island species (25) and also among invertebrate animal Within that context, two major classes of adaptive benefithave taxa (26)—between proclivity to self-fertilize and colonization been argued to help explain selfing’s evolutionary maintenance. potential. Baker argued that self-fertilization is advantageous in The first hypothesis follows logically from the severe restriction on any hermaphroditic species in which opportunities for outcrossing genetic recombination that self-fertilization promotes (7). When are constrained for any reason, such as low population density selfing predominates in a sexual population for even a few gen- (e.g., in newly colonized habitats), unequal sex ratio, or any other erations, heterozygosity rapidly decays (homozygosity increases) ecological or genetic basis for a paucity of suitable mates. We such that relatively little intraindividual genetic variation soon henceforth refer to fertilization assurance as Baker’s contention remains available for shuffling into novel multilocus allelic suites. for the adaptive significance of selfing. Allard’s argument and In the extreme, reproduction within a highly inbred lineage in ef- Baker’s contention are not mutually exclusive (i.e., both could fect becomes “clonal” as highly homozygous individuals self-fer- apply to a given species), but they do convey different sentiments tilize in successive generations and thereby produce essentially about fitness dividends from self-fertilization. Under Allard’s ar- isogenic (genetically identical) offspring. Although meiosis and gument, selfing’s restraint on genetic recombination is the key syngamy continue to operate in a selfing lineage, these cellular evolutionary factor, whereas Baker’s scenario emphasizes in- processes become ineffective in generating recombinant geno- herent benefits of selfing that derive from assured fertilization. types; instead, multilocus isogenotypes favored by natural selec- Table 1 summarizes several other implications of Baker’s tion tend to be preserved and proliferate (Fig. 1). contention versus Allard’s argument. For example, the former In the early 1970s, Robert Allard and colleagues published implies that selection might act to favor even a single gene that seminal articles empirically documenting how selfing’s restriction promotes self-fertilization, whereas the latter invokes co- on genetic recombination can act in conjunction with natural se- adaptation at the genomic level. Thus, although fertilization as- lection to favor the spread of coadapted multilocus suites of surance (Baker’s contention) offers immediate fitness payoffs to alleles well molded to local ecological conditions (7, 8–11). These studies involved plant populations with predominant selfing and showed that particular multilocus genotypes routinely reached Author contributions: J.C.A. and A.T. designed research; J.C.A. and A.T. performed re- substantial frequencies in populations with high self-fertilization search; A.T. contributed new reagents/analytic tools; A.T. analyzed data; and J.C.A. wrote rates. Furthermore, as summarized by Allard et al. (12), “these the paper. multiallelic configurations are distributed ecogeographically in The authors declare no conflict of interest. patchwork patterns that are precise overlays of environmental 1To whom correspondence should be addressed. E-mail: [email protected]. 18862–18867 | PNAS | November 13, 2012 | vol. 109 | no. 46 www.pnas.org/cgi/doi/10.1073/pnas.1217202109 Downloaded by guest on September 25, 2021 selfing relative generation H selfing lineages 0 1.00 A- B- C- D- E- F- G- H- I- J- 1 0.50 A- B- C- D- E- F- G- H- I- J- 2 0.25 A- B- C- D- E- F- G- H- I- J- 3 0.12 A- B- C- D- E- F- G- H- I- J- 4 0.06 A- B- C- D- E- F- G- H- I- J- 5 0.03 AA BB CC DD EE FF GG HH II JJ 6 0.02 BB BB CC EE EE EE GG HH JJ JJ 7 0.01 BB BB EE EE EE EE EE EE JJ JJ 8 <0.01 BB BB EE EE EE EE EE EE EE JJ Fig. 1. Expected declines in population H 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). any self-fertile individual in each generation, especially when argument implies that particular multilocus genotypes should mating opportunities are limited, Allard’s argument entails de- reach moderate to high frequencies in habitats where they are fi fi fi ’ ferred tness bene ts because several generations of sel ng and locally well adapted. Empirically, in Allard s self-fertilizing plants EVOLUTION natural selection must transpire before a formerly outcrossed and in Selander’s self-fertilizing snails, different multilocus lineage might evolve multilocus coadaptation (either inside the genotypes consistently characterized local populations occupying genome or in relation to external ecological niches). Further- xeric versus mesic environments. By contrast, Baker’s scenario more, further outcrossing effectively disintegrates (via genetic necessitates no epistasis and no particular association between recombination) any coadapted
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