Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish.

Turner, Bruce J.; Elder, John F.; Laughlin, Thomas F.; Davis, William P.; Taylor, D. Scott

doi:10.1073/pnas.89.22.10643

Cited by 90 publications

(59 citation statements)

References 15 publications

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“…Differences in low-temperature male induction as well as morphological anomalies among seven other clones from Florida to Brazil have also been observed (Turner 2003 1 ). In the field, Turner et al (1990Turner et al ( , 1992a used DNA fingerprinting to confirm both high levels of intrapopulation genetic heterogeneity and clonal variation in three Harrington-Kallman clones of Rivulus marmoratus. All of these studies demonstrate the high phenotypic and genetic variability of this species.…”

Section: Clonal Heterogeneity As An Adaptive Strategymentioning

confidence: 99%

Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus

et al. 2005

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SynopsisWe compared life-history traits such as fecundity, sex ratio, reproductive cycle, age at sexual maturity, embryonic period, egg size, early growth and morphology in two clonal strains (PAN-RS and DAN) of the mangrove killifish (Rivulus marmoratus) under constant rearing conditions. We found a positive relationship between growth and reproductive effort. Fecundity was significantly higher in the PAN-RS strain than in the DAN strain. Sex ratio was significantly different, with DAN producing more primary males than PAN-RS. Spawning and ovulation cycle did not clearly differ between the strains. PAN-RS showed a significantly higher growth rate than DAN from 0 to 100 days after hatching, however, age at sexual maturity, embryonic period, egg size, and morphometric and meristic characteristics (vertebral and fin-ray counts) did not differ between the two strains. The high fecundity of PAN-RS may provide an increased chance of offspring survival, while the attainment of sexual maturity at a smaller size in DAN may allow them to invest earlier in reproduction to increase breeding success.Variations in the life-history traits of PAN-RS and DAN may be adaptive strategies for life in their natural habitat, which consists of mangrove estuaries with a highly variable environment. 2 IntroductionThe individual traits of organisms and their interaction with the environment define the dynamics of populations, the structure of ecological communities, and the functioning of ecosystems (Tessier et al. 2000). Identifying trends in life-history traits and interpreting the adaptiveness of such variation has always been a challenge for biologists (Stearns 1992). It is generally believed that observed differences in life-history traits result from genotypic variation and/or from the effect on a plastic phenotype of variation in the environment (Belk 1995). One of the most important issues in evolutionary biology is defining whether differences in life-history traits can be attributed to genetic or environmental variation.In the present study, we used two clonal strains of mangrove killifish (Rivulus marmoratus, Family Rivulidae) to identify differences in life-history traits and determine whether these variations are the result of genetic or environmental differences.The mangrove killifish is distributed from Southern Florida, U.S.A. to Brazil (Davis et al. 1990). It inhabits mangrove areas, which are exposed to alternate flooding and desiccation; thus, it is necessarily tolerant of a wide range of environmental conditions (Taylor 2000). There are three recognized sexual types: hermaphrodites, which have a marbled brownish color pattern usually including a caudal ocellus, and are capable of internal synchronous self-fertilization, and thus are capable of producing clonal lineages (Kallman & Harrington 1964, Harrington & Kallman 1968; primary males, which have an orange body coloration usually without caudal ocellus and remain male throughout their lives; and secondary males, which arise from hermaphrodites following the loss o...

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Section: Clonal Heterogeneity As An Adaptive Strategymentioning

confidence: 99%

Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus

et al. 2005

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“…Simultaneous hermaphroditism and self-fertilization in K. marmoratus were discovered in the 1960s (3). 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).…”

mentioning

confidence: 99%

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

Tatarenkov

Lima

Taylor³

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

108

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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

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“…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).…”

mentioning

confidence: 99%

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

Mackiewicz

Tatarenkov

Taylor³

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

121

147

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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...

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Extreme clonal diversity and divergence in populations of a selfing hermaphroditic fish.

Abstract: Recombination is unknown in natural popu-

Cited by 90 publications

References 15 publications

Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus

Differences in life-history traits in two clonal strains of the self-fertilizing fish, Rivulus marmoratus

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

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

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