The mangrove killifish (Kryptolebias marmoratus) is the only vertebrate known to be capable of self-fertilization. Its gonad is typically an ovotestis that simultaneously produces eggs and sperm, and fertilization is internal. Although most populations of this species consist primarily or exclusively of hermaphroditic individuals, gonochoristic males occur at Ϸ20% frequency in a natural population at Twin Cays, Belize. Here we use a battery of 36 microsatellite loci to document a striking genetic pattern (high intraspecimen heterozygosities and low within-population linkage disequilibria) that differs qualitatively from the highly homozygous (or ''clonal'') genetic architecture characteristic of killifish populations previously studied in Florida, where males are much rarer. These findings document that outcrossing (probably between gonochoristic males and hermaphrodites) is common at the Belize site, and, more importantly, they demonstrate the dramatic impact that functional androdioecy can have on the population genetic architecture of this reproductively unique vertebrate species.A ndrodioecy is a rare reproductive system in which a natural population consists of functional males and hermaphrodites but no true female gonochorists. Previously known only in a few plants (1-10) and invertebrate animals (11-15), androdioecy has also evolved independently in a vertebrate species: the mangrove killifish, Kryptolebias (formerly Rivulus) marmoratus. Most surveyed populations of K. marmoratus consist primarily or exclusively of hermaphroditic individuals, but gonochoristic males are observed occasionally, and recent genetic evidence suggests that such individuals may mediate infrequent outcross events in this otherwise self-fertilizing species (16-18). The net result, documented most clearly for Florida locales (16), is a mixed-mating population genetic architecture consisting mostly of highly homozygous inbred strains (traditionally referred to as ''clones'') plus low percentages of highly heterozygous specimens stemming from recent outcross events. Thus, the genetic variety generated by outcrossing (16), and subsequently converted into new arrays of recombinant inbred lines upon resumptions of selfing, can significantly augment mutation and interlocality gene flow that formerly were thought to be the sole sources of ''clonal'' diversity in K. marmoratus (19)(20)(21).Gonochoristic males, which are phenotypically recognizable by coloration and histology, seem to be extremely rare in Florida (in our experience, Ͻ1% frequency among Ͼ1,000 individuals examined). However, in a collection from Twin Cays, Belize, made during 1988 and 1989, 53 males (18.8%) were present among 282 specimens surveyed (22). In laboratory-reared progeny from another collection (in 1991) of hermaphrodites from this Belize locale, segregating genetic variation was detected, a result interpreted to imply that natural outcrossing had occurred between males and hermaphrodites (17, 18).In this study, we use a battery of 36 microsatellite loci to exami...
Although first described in 1880, Kryptolebias marmoratus avoided scientific scrutiny until 1961, when it was identified as the only known selfing hermaphroditic vertebrate. The subsequent intense interest in this fish as a laboratory animal, continuing to this day, might explain the paucity of wild collections, but our collective knowledge now suggests that the inherent difficulty of wild collection is more a matter of "looking in all the wrong places." Long thought to be rare in the mangroves, and it is rare in certain human-impacted habitats, K. marmoratus can be quite abundant, but in microhabitats not typically targeted by ichthyologists: ephemeral pools at higher elevations in the swamp, crab burrows, and other fossorial or even terrestrial haunts. Field studies of this enigmatic fish have revealed almost amphibious behaviors. During emersion these fish tolerate extended dry periods. In water, they are exposed to temperature extremes, high levels of hydrogen sulfide, and depleted dissolved oxygen. Finally, their catholic diet and a geographically variable sex life completes a portrait of an unusual animal. A clearer picture is emerging of adult life, with initial population density estimates now known and some indication of high population turnover in burrows, but juvenile habitat and adult oviposition sites remain unknown.
We use extensive geographical sampling and surveys of nuclear microsatellite and mitochondrial DNA loci to investigate the phylogeographic structure of the only recognized self-fertilizing vertebrates, the mangrove killifishes, currently thought to comprise two cryptic species, Kryptolebias marmoratus and Kryptolebias hermaphroditus. All genetic markers revealed three concordant main clades. The Northern clade includes populations from Florida, northern Cuba, Bahamas, Belize and Honduras and corresponds to K. marmoratus. The Southern clade encompasses populations from Brazil and corresponds to K. hermaphroditus. This species was considered endemic to southeastern Brazil, but molecular data corroborate its occurrence in northeastern Brazil. The Central clade, not previously resolved with genetic data, includes populations from Panama and Antilles. Despite the geographic proximity of the Northern and Central clades, the latter is genetically closer to the Southern clade. The discovery of the Central clade raises some taxonomic issues -it can either be considered a distinct species or united with the Southern clade into a single species with two subspecies. Another possible taxonomic solution is a single selfing species, K. marmoratus, with three subspecies. We show that the Central and Southern clades are highly selfing (97-100%), whereas selfing rates of the Northern clade populations vary geographically (39-99%). Genetic patterns indicate that populations in SE Brazil are recent, contrary to expectations based on the known distributions of related species.
Among vertebrate animals, only the mangrove rivulus (Kryptolebias marmoratus) was known to self-fertilize. Here, we use microsatellite analyses to document a high selfing rate (97%) in a related nominal species, Kryptolebias ocellatus, which likewise is androdioecious (populations consist of males and hermaphrodites). In contrast, we find no evidence of self-fertilization in Kryptolebias caudomarginatus (an androdioecious species closely related to the marmoratus-ocellatus clade) or in Kryptolebias brasiliensis (a dioecious outgroup). These findings indicate that the initiation of self-fertilization predated the origin of the marmoratus-ocellatus clade. From mitochondrial DNA sequences and microsatellite data, we document a substantial genetic distance between Kryptolebias marmoratus and K. ocellatus, implying that the selfing capacity has persisted in these fishes for at least several hundred thousand years.androdioecy ͉ hermaphroditism ͉ mangrove killifish ͉ mating systems ͉ reproductive modes
The mangrove rivulus Kryptolebias marmoratus and a closely related species are the world's only vertebrates that routinely self-fertilize. Such uniqueness presents a model for understanding why this reproductive mode, common in plants and invertebrates, is so rare in vertebrates. A survey of 32 highly polymorphic loci in >200 specimens of mangrove rivulus from multiple locales in the Florida Keys, USA, revealed extensive population-genetic structure on microspatial and micro-temporal scales. Observed heterozygosities were severely constrained, as expected for a hermaphroditic species with a mixed-mating system and low rates of outcrossing. Despite the pronounced population structure and the implied restrictions on effective gene flow, isogenicity (genetic identity across individuals) within and among local inbred populations was surprisingly low even after factoring out probable de novo mutations. Results indicate that neither frequent bottlenecks nor directional genetic adaptation to local environmental conditions were the primary driving forces impacting multilocus population-genetic architecture in this self-fertilizing vertebrate species. On the other hand, a high diversity of isogenic lineages within relatively small and isolated local populations is consistent with the action of diversifying selection driven by the extreme spatio-temporal environmental variability that is characteristic of mangrove habitats.
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