The mangrove rivulus

Mangrove rivulus hermaphrodite (foreground) and male (background)

At a first glance, mangrove rivulus appears like ordinary fish. However, this species possesses an extraordinary life-history that has been the subject of interest of many scientists since its discovery.

The mangrove rivulus, Kryptolebias marmoratus, is found over a huge geographic range, comprising the coastal lines of Central America, Southern North America to the mouth of Amazon River in South America. It is closely affiliated with the red mangrove Rhizophora mangle.

Major habitats of mangrove rivulus are burrows excavated by land crabs. The abiotic conditions in the burrows are highly variable, fluctuating with tides, weather and seasons. They’re characterized by generally low dissolved oxygen, high levels of hydrogen sulfide from rotting mangrove leaves and a fluctuating salinity.

A big male rivulus found on Twin Caye, Belize.

The first amazing fact about this fish is that they are not bothered at all by these harsh conditions. When the conditions become too extreme, they even emerse and they are able to live out of water for more than 2 months. The cues that trigger emersion are high levels of H2S, low dissolved O2, hunger, drought, or agression from other fish.  They stay in moist leaf litter or in insect tunnels within rotting logs. While out of water, the skin takes the function of the gills : dense networks of blood vessels below the surface of the skin allows the uptake of oxygen. This species displays thus high levels of phenotypic plasticity, which is the fact that a given genotype can lead to different phenotypes depending on the environmental conditions.

The second surprising fact is their mode of reproduction. They are the only vertebrates known to be hermaphrodites and able to self-fertilize. Long bouts of self-fertilization lead to genetically identic homozygous lineages. Males occur in some populations, allowing some sexual outcrossing with hermaphrodites and increasing genetic diversity. There is no female. The simultaneous occurance of males and hermaphrodites is called androdioecy.

For these two reasons, the mangrove rivulus provides an excellent model for the study of phenotypic plasticity. First, we can probably get more information about a species able to survive at the limits of tolerance (showing a high phenotypic plasticity) than one tolerating a narrow range of environmental conditions. Second, the avaibility of isogenic lineages eliminates the effect of genetic variability when looking at the effects of the environment on the phenotype.

Searching for rivulus in the mangroves on Long Caye, Belize

The self-fertilizing mangrove rivulus as a model species in environmental epigenetics

Phenotypic variation is known to arise from genetic diversity, environmental variability and their interaction. However, there is an increasing body of evidences that heritable epigenetic variation can also contribute to phenotypic changes in a population. A deeper understanding of the roles of epigenetic mechanisms in phenotypic diversity and, consequently, in organism adaptation and evolution, can only be achieved in individuals that are genetically identical but naturally exhibit a range of heritable phenotypes. For that purpose, the mangrove rivulus, Kryptolebias marmoratus, is a precious model species. Closely associated to the red mangrove Rhizophora mangle forests from Florida to South America, it shows numerous adaptations to live in environment with considerable variability in terms of oxygen, temperature, salinity, or toxicants levels. Beside its ability to survive several weeks out of water, its main biological particularity is its mixed-mating reproduction system including portions of self- and cross-fertilization. Depending on the regions, the ratio between hermaphrodites and males varies together with the selfing rate (high selfing when males are rare), which directly affects the genetic diversity. In our research projects, we show that mangrove rivulus is a valuable model to understand the role of epigenetics in phenotypic variability. Using methods such as Luminometric Methylation Assay or Reduced Representation Bisulfite Sequencing, we characterized the DNA methylation reprogramming during embryogenesis, a presumed sensitive window to environmental cues. Differentially methylated fragments were associated to specific behavioral traits such as boldness and aggressiveness. Effects of exposure to different environmental contaminants, such as neurotoxicant compounds (NCs) or endocrine disrupting chemicals (EDCs), during early life stages or adulthood, were assessed in order to investigate the relation between DNA methylation and the phenotype. Recently, we also studied four natural populations, in Belize and in Florida, within a gradient of genetic diversity. We could therefore lay the foundations of epigenetic studies at the population level and open the door to future researches about the role of DNA methylation in the evolution of populations with very low genetic diversity.
In conclusion, this model allows researchers to distinguish epigenetic from genetic contributions to explain phenotypic plasticity.

 

Follow this link to read an excellent outreach article about our researches on the rivulus, published on the UNamur Newsroom.

Personal pictures of the mangrove rivulus can be found here.

Documentary about searching for the mangrove rivulus can be watched here.

 

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