Divergent and non-parallel evolution of MHC IIB in the Neotropical Midas cichlid species complex.

BACKGROUND: Ecological diversification is the result of divergent natural selection by contrasting habitat characteristics that favours the evolution of distinct phenotypes. This process can happen in sympatry and in allopatry. Habitat-specific parasite communities have the potential to drive diversification among host populations by imposing selective pressures on their host's immune system. In particular, the hyperdiverse genes of the major histocompatibility complex (MHC) are implicated in parasite-mediated host divergence. Here, we studied the extent of divergence at MHC, and discuss how it may have contributed to the Nicaraguan Midas cichlid species complex diversification, one of the most convincing examples of rapid sympatric parallel speciation. RESULTS: We genotyped the MHC IIB for individuals from six sympatric Midas cichlid assemblages, each containing species that have adapted to exploit similar habitats. We recovered large allelic and functional diversity within the species complex. While most alleles were rare, functional groups of alleles (supertypes) were common, suggesting that they are key to survival and that they were maintained during colonization and subsequent radiations. We identified lake-specific and habitat-specific signatures for both allelic and functional diversity, but no clear pattern of parallel divergence among ecomorphologically similar phenotypes. CONCLUSIONS: Colonization and demographic effects of the fish could have contributed to MHC evolution in the Midas cichlid in conjunction with habitat-specific selective pressures, such as parasites associated to alternative preys or environmental features. Additional ecological data will help evaluating the role of host-parasite interactions in the Midas cichlid radiations and aid in elucidating the potential role of non-parallel features differentiating crater lake species assemblages.

Systematics and Taxonomy of Tonatia saurophila Koopman & Williams, 1951 (Chiroptera, Phyllostomidae).

The Stripe-headed Round-eared bat, Tonatia saurophila, includes three subspecies: Tonatia saurophila saurophila (known only from subfossil records in Jamaica), Tonatia saurophila bakeri (distributed from southeastern Mexico to northern Colombia, Venezuela west and north of the Cordillera de Mérida, and northwestern Ecuador), and Tonatia saurophila maresi (distributed in Venezuela east and south of the Cordillera de Mérida, the Guianas, Trinidad and Tobago, northeastern Brazil, and along the upper Amazon basin in Colombia, Ecuador, Peru, and Bolivia). The last two subspecies are an attractive example to test predictions about the historical role of the Andes in mammalian diversification. Based on morphological descriptions, morphometric analyses, and phylogenetic reconstruction using the mitochondrial gene Cyt-b and the nuclear exon RAG2, this study evaluates the intraspecific relationships within Tonatia saurophila and the taxonomic status of the taxon. The three subspecies of T. saurophila are recognizable as full species: Tonatia bakeri, Tonatia maresi, and Tonatia saurophila. The latter is restricted to its type locality and possibly is extinct. Tonatia bakeri, in addition to being larger than T. maresi, is morphologically distinguishable by possessing an acute apex at the posterior edge of the skull, a well-developed clinoid process, and relatively robust mandibular condyles, and by lacking a diastema between the canine and the first lower premolar. The genetic distance between T. bakeri and T. maresi is 7.65%.

ResumenEl Murciélago de orejas redondas de cabeza rayada, Tonatia saurophila, incluye tres subespecies: Tonatia saurophila saurophila (conocida sólo por registros subfósiles en Jamaica), Tonatia saurophila bakeri (distribuida desde el sureste de México hasta el norte de Colombia, Venezuela al oeste y norte de la Cordillera de Mérida, y el noroeste de Ecuador), y Tonatia saurophila maresi (distribuida en Venezuela al este y sur de la Cordillera de Mérida, las Guayanas, Trinidad y Tobago, el noreste de Brasil, y la vertiente amazónica de los Andes de Colombia, Ecuador, Peru y Bolivia). Las dos últimas subespecies representan un ejemplo atractivo para poner a prueba predicciones sobre el rol histórico de los Andes en la diversificación de mamíferos. Con base en descripciones morfológicas, análisis morfométricos y una reconstrucción filogenética empleando el gen mitocondrial Cyt-b y el gen nuclear RAG2, este estudio evalúa las relaciones intraspecíficas dentro de Tonatia saurophila y el estatus taxonómico del taxón. Las tres subespecies de T. saurophila son reconocidas como especies plenas: Tonatia bakeri, T. maresi y T. saurophila. Esta última está restringida a la localidad tipo y posiblemente está extinta. Tonatia bakeri, además de ser de mayor tamaño que T. maresi, se diferencia morfológicamente por poseer un ápice agudo en el borde posterior del cráneo, un proceso clinoideo bien desarrollado y cóndilos mandibulares relativamente robustos, y por carecer de un diastema entre el canino y el primer premolar inferior. La distancia genética entre T. bakeri y T. maresi es 7.65%.

An exploration of the links between parasites, trophic ecology, morphology, and immunogenetics in the Lake Tanganyika cichlid radiation.

Differences in habitat and diet between species are often associated with morphological differences. Habitat and trophic adaptation have therefore been proposed as important drivers of speciation and adaptive radiation. Importantly, habitat and diet shifts likely impose changes in exposure to different parasites and infection risk. As strong selective agents influencing survival and mate choice, parasites might play an important role in host diversification. We explore this possibility for the adaptive radiation of Lake Tanganyika (LT) cichlids. We first compare metazoan macroparasites infection levels between cichlid tribes. We then describe the cichlids' genetic diversity at the major histocompatibility complex (MHC), which plays a key role in vertebrate immunity. Finally, we evaluate to what extent trophic ecology and morphology explain variation in infection levels and MHC, accounting for phylogenetic relationships. We show that different cichlid tribes in LT feature partially non-overlapping parasite communities and partially non-overlapping MHC diversity. While morphology explained 15% of the variation in mean parasite abundance, trophic ecology accounted for 16% and 22% of the MHC variation at the nucleotide and at the amino acid level, respectively. Parasitism and immunogenetic adaptation may thus add additional dimensions to the LT cichlid radiation.

Molecular characterization of MHC class IIB genes of sympatric Neotropical cichlids.

BACKGROUND: The Major Histocompatibility Complex (MHC) is a key component of the adaptive immune system of all vertebrates and consists of the most polymorphic genes known to date. Due to this complexity, however, MHC remains to be characterized in many species including any Neotropical cichlid fish. Neotropical crater lake cichlids are ideal models to study evolutionary processes as they display one of the most convincing examples of sympatric and repeated parallel radiation events within and among isolated crater lakes. RESULTS: Here, we characterized the genes of MHC class IIB chain of the Midas cichlid species complex (Amphilophus cf. citrinellus) including fish from five lakes in Nicaragua. We designed 19 new specific primers anchored in a stepwise fashion in order to detect all alleles present. We obtained 866 genomic DNA (gDNA) sequences from thirteen individuals and 756 additional sequences from complementary DNA (cDNA) of seven of those individuals. We identified 69 distinct alleles with up to 25 alleles per individual. We also found considerable intron length variation and mismatches of alleles detected in cDNA and gDNA suggesting that some loci have undergone pseudogenization. Lastly, we created a model of protein structure homology for each allele and identified their key structural components. CONCLUSIONS: Overall, the Midas cichlid has one of the most diverse repertoires of MHC class IIB genes known, which could serve as a powerful tool to elucidate the process of divergent radiations, colonization and speciation in sympatry.