Deep and concordant subdivisions in the self-fertilizing mangrove killifishes (Kryptolebias) revealed by nuclear and mtDNA markers

Abstract

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.

Local parasite pressures and host genotype modulate epigenetic diversity in a mixed‐mating fish

“…We found that the different selfing lineages of Kryptolebias hermaphroditus distributed in three sampling sites of northeastern Brazil differed significantly in parasite loads, genetic composition, and DNA methylation patterns, which might indicate specific interactions between host genotypes, epigenotypes, and parasites (Dybdhal & Lively, ; Ebert, ). Previous studies on mangrove killifishes had identified extensive genetic structuring both between (Tatarenkov et al, , ) and within mangrove systems even at close geographical proximity (Ellison et al, ; Tatarenkov, Earley, Taylor, & Avise, ; Tatarenkov et al, ), as a consequence of the self‐fertilizing nature of these fish. We found strong evidence of genetic structuring between sampling sites and selfing lineages using microsatellites, but lower differentiation for AFLP genetic markers (likely due to the different mutation rate of the markers) and epigenetic markers (MS‐AFLPs).…”

“…A total of 128 specimens of K. hermaphroditus were collected using hand‐nets from three sampling sites on isolated mangroves on the northeastern coast of Brazil between January and September 2015: Ceará‐Mirim River—Site 1; Curimataú River—Site 2; Ipojuca River—Site 3 (Figure ). K. hermaphroditus is distributed along the Brazilian coast (Tatarenkov et al, ) and is typically found in shallow pools of high salinity levels (>30 ppt), clear waters, and muddy substrates, where there are few other sympatric fish (Berbel‐Filho et al, ; Lira, Paiva, Ramos, & Lima, ). All specimens displayed the common hermaphrodite phenotype (dark color with well‐defined ocellus on the caudal fin; Costa, ).…”

“…Gills are an important physical and immunological barrier to pathogens in fish (Press & Evensen, ) and the organ where most parasites were found (Table ). Twenty‐seven microsatellite loci (Mackiewicz et al, ; Tatarenkov et al, ) were genotyped as in Ellison et al () and screened using GeneMapper v.4.0 (Applied Biosystems). Loci were tested for linkage disequilibrium and Hardy–Weinberg equilibrium using GENEPOP v. 4.5.1 (Rousset, ).…”

“…marmoratus and K . hermaphroditus ), characterized by variable rates of selfing and outcrossing (Tatarenkov et al, ). Populations of both species consist mainly of self‐fertilizing hermaphrodites and varying levels of males at low frequencies (Berbel‐Filho, Espirito‐Santo, & Lima, ; Tatarenkov et al, ), and exhibit high levels of homozygosity (Tatarenkov et al, ; Tatarenkov, Lima, Taylor, & Avise, ), suggesting that self‐fertilization is the most common mode of reproduction (Avise & Tatarenkov, ).…”

Updated checklist and DNA barcode‐based species delimitations reveal taxonomic uncertainties among freshwater fishes from the mid‐north‐eastern Caatinga ecoregion, north‐eastern Brazil

“…The mangrove killifish K. hermaphroditus is broadly distributed within mangrove microhabitas along the Brazilian coast (Lira et al ., ; Tatarenkov et al . ).…”