Extensive outcrossing and androdioecy in a vertebrate species that otherwise reproduces as a self-fertilizing hermaphrodite

Abstract

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...

Long-term retention of self-fertilization in a fish clade

“…Nevertheless, we present a vertebrate lineage in which simultaneous hermaphroditism has arisen and persisted for at least hundreds of thousands of years. However, self-fertilization is merely a component of a mixed-mating system in Kryptolebias (9)(10)(11)(12), where various populations self-fertilize and outcross at different rates. Although Kryptolebias fishes provide the only known examples of mixed-mating systems in vertebrate animals, such systems are relatively common in many plants and invertebrate taxa (4).…”

“…Later, researchers used molecular markers to confirm self-fertilization in this species (8) and to derive the first quantitative estimates of selfing and outcrossing rates (9)(10)(11)(12). The latter vary geographically; outcrossing rates are high (Ϸ50%) in some Belize islands where males are common but low (Ͻ3%) in Florida and the Bahamas where males are rare (11)(12)(13)(14).…”

No amicable divorce? Challenging the notion that sexual antagonism drives sex chromosome evolution

“…Gynodioecy occurs in cnidarians [82][83][84] but is unknown in triploblastic animals. Androdioecy is slightly more common, occurring in branchiopod crustaceans [85], rhabditid nematodes [86] and a single vertebrate species, the mangrove killifish [87], but these androdioecious species appear to have evolved from dioecious ancestors rather than from hermaphrodites [88]. Androdioecy also occurs in barnacles where it is unclear whether it evolved from hermaphroditism or from dioecy [89].…”

Allard's argument versus Baker's contention for the adaptive significance of selfing in a hermaphroditic fish

“…31). The following are some of genetic discoveries made across the years about these unique fish: (i) selfing lineages in Kmar do exhibit genetic variation, albeit at reduced levels compared with most outcrossing species (32-37); (ii) males as well as hermaphrodites exist in some populations (38,39), thus making Kmar an androdioecious species (40); (iii) these males sometimes mediate outcross events (41) such that Kmar has a mixed-mating system (40,42,43) with predominant selfing; and (iv) these and other features of the reproductive system have been mapped phylogenetically and phylogeographically across members of the Kmar clade to yield inferences about evolutionary histories of the self-fertilization syndrome (27,44,45). …”