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Ecological and evolutionary consequences of alternative sex-change pathways in fish.

ABSTRACT: Sequentially hermaphroditic fish change sex from male to female (protandry) or vice versa (protogyny), increasing their fitness by becoming highly fecund females or large dominant males, respectively. These life-history strategies present different social organizations and reproductive modes, from near-random mating in protandry, to aggregate- and harem-spawning in protogyny. Using a combination of theoretical and molecular approaches, we compared variance in reproductive success (V k*) and effective population sizes (N e) in several species of sex-changing fish. We observed that, regardless of the direction of sex change, individuals conform to the same overall strategy, producing more offspring and exhibiting greater V k* in the second sex. However, protogynous species show greater V k*, especially pronounced in haremic species, resulting in an overall reduction of N e compared to protandrous species. Collectively and independently, our results demonstrate that the direction of sex change is a pivotal variable in predicting demographic changes and resilience in sex-changing fish, many of which sustain highly valued and vulnerable fisheries worldwide.

SUBMITTER: Benvenuto C

PROVIDER: S-EPMC5567342 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Ecological and evolutionary consequences of alternative sex-change pathways in fish.

Benvenuto C C Coscia I I Chopelet J J Sala-Bozano M M Mariani S S

Scientific reports 20170822 1

Sequentially hermaphroditic fish change sex from male to female (protandry) or vice versa (protogyny), increasing their fitness by becoming highly fecund females or large dominant males, respectively. These life-history strategies present different social organizations and reproductive modes, from near-random mating in protandry, to aggregate- and harem-spawning in protogyny. Using a combination of theoretical and molecular approaches, we compared variance in reproductive success (V <sub>k</sub> ...[more]

PMID: 28831108

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Project description:Background and aimsThe outbreeding floral polymorphism heterostyly frequently breaks down, resulting in the evolution of self-fertilization as a result of homostyle formation. Here, the loss of floral polymorphism in distylous Primula oreodoxa, a sub-alpine species restricted to western Sichuan, China, was examined by investigating the ecological correlates and genetic consequences of mating system transitions. Several key questions were addressed. (1) What are the frequencies, geographical distribution and reproductive characteristics of floral morphs in distylous and homostylous populations? (2) Does increased elevation influence pollinator service and the likelihood of inbreeding in populations? (3) How often has homostyly originated and what are the consequences of the breakdown of distyly for the amounts and distribution of genetic diversity in populations?MethodsFourteen populations throughout the range of P. oreodoxa were sampled, and morph frequencies and floral characteristics were recorded. Polymorphism at microsatellite loci and chloroplast DNA (cpDNA) variation were used to quantify population genetic structure and genetic relationships among populations. Controlled pollinations and studies of pollen tube growth and fertility were conducted to determine the compatibility status of populations and their facility for autonomous self-pollination. Finally, visitation rates of long- and short-tongued pollinators to distylous and homostylous populations at different elevations were compared to determine if increased elevation was associated with deterioration in pollinator service.Key resultsIn contrast to most heterostylous species, both distylous and homostylous morphs of P. oreodoxa are highly self-compatible, but only homostyles have the facility for autonomous self-pollination. Homostyles set significantly more fruit and seeds following open pollination than the distylous morphs. Visitation by long-tongued pollinators was significantly lower in homostylous populations, and overall rates of insect visitation decreased with elevation. Genetic diversity was significantly lower in homostylous populations, with evidence of increased inbreeding at higher elevation. Patterns of cpDNA variation were consistent with multiple transitions from distyly to homostyly and limited gene flow among populations.ConclusionsThe results of this study support the hypothesis that the multiple loss of floral polymorphism in distylous P. oreodoxa is associated with unsatisfactory pollinator service, with homostyles benefiting from reproductive assurance as a result of autonomous self-pollination.

Project description:When facing environmental change and intensified anthropogenic impact on marine ecosystems, extensive knowledge of how these systems are functioning is required in order to manage them properly. However, in high-latitude ecosystems, where climate change is expected to have substantial ecological impact, the ecosystem functions of biological species have received little attention, partly due to the limited biological knowledge of Arctic species. Functional traits address the ecosystem functions of member species, allowing the functionality of communities to be characterised and the degree of functional redundancy to be assessed. Ecosystems with higher functional redundancy are expected to be less affected by species loss, and therefore less sensitive to disturbance. Here we highlight and compare typical functional characteristics of Arctic and boreal fish in the Barents Sea and address the consequences of a community-wide reorganization driven by climate warming on functional redundancy and characterization. Based on trait and fish community composition data, we assessed functional redundancy of the Barents Sea fish community for the period 2004-2012, a period during which this northern region was characterized by rapidly warming water masses and declining sea ice coverage. We identified six functional groups, with distinct spatial distributions, that collectively provide a functional characterization of Barents Sea fish. The functional groups displayed different prevalence in boreal and Arctic water masses. Some functional groups displayed a spatial expansion towards the northeast during the study period, whereas other groups showed a general decline in functional redundancy. Presently, the observed patterns of functional redundancy would seem to provide sufficient scope for buffering against local loss in functional diversity only for the more speciose functional groups. Furthermore, the observed functional reconfiguration may affect future ecosystem functioning in the area. In a period of rapid environmental change, monitoring programs integrating functional traits will help inform management on ecosystem functioning and vulnerability.

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Ecological and evolutionary consequences of alternative sex-change pathways in fish.

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Ecological and evolutionary consequences of alternative sex-change pathways in fish.

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