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A central question in ecology and evolution is how standing variation in natural populations is maintained, and how divergent natural selection shapes this variation into adaptive differences between populations and species. The Trinidadian guppy, Poecilia reticulata, represents one of the best vertebrate models for the study of how phenotypic variation within a population is linked to adaptation to specific environmental conditions. Guppies are well known for the highly polymorphic color patterns of the males that have been a subject of genetic analysis for almost a century (Winge, J. Genet. 18, 1, 1927). David Reznick and colleagues have studied these populations in the wild for many years, focusing on their ecogeographic adaptations to different river habitats. Upper and lower river populations in several drainages in Northern Trinidad are separated by barrier waterfalls and have developed different adaptive traits that are known to depend on the presence or absence of predators, among other environmental factors. Distinguishing traits include courtship and mating behavior, conspicuous color patterns of males, age and size at maturity, brood intervals and brood size. Despite the wealth of field studies and the availability of feral as well as inbred strains, knowledge of the mechanistic foundation of these phenomena is scarce to non-existent.

The vast literature on its ecology and evolution and the extensive phenotypic variation in wild populations make the guppy a particularly attractive choice for understanding the molecular basis for adaptation to varying natural conditions. The long-term goal of this project, which has been jointly initiated by the Dreyer and Weigel groups with considerable help from collaborators Reznick and Breden, is to uncover the genes underlying the phenotypic variation that is the raw material for selection. As a first step, genomic resources have been generated. cDNA libraries have been produced from several tissues and strains and EST sequences have been assembled in a database that currently comprises 18.000 entries, representing 6000 different ESTs. Further, about 0.5% of the genome has been analyzed by end sequencing of BAC clones from a genomic library of male Cumaná guppies. Crosses between wild-collected guppies from geographically distant locations in Trinidad and Venezuela showed that the majority of hybrids could produce viable and fertile F2 offspring, despite some indications for incipient reproductive isolation.

A genetic linkage map comprising more than 700 markers on 23 linkage groups (corresponding to the known haploid chromosome number) has been constructed, based on single nucleotide polymorphisms (SNPs) found in expressed genes and in genomic DNA sequenced at random (Namita Tripathi). The same markers have also been used to genotype a collection of different wild guppy strains from Trinidad and Venezuela (Eva Willing).

After mapping of QTL that control male ornaments and body shape, we will aim at mapping QTL underlying the more subtle variation that shapes adaptation to different habitats in the wild.

A major challenge remains the fine mapping and functional analysis of the color trait loci found in the gonosomal region of the Y chromosome, and their relationship to the the sex-determining locus itself.

In addition, candidate genes for specification, migration and differentiation of pigment cells in male guppies are being examined. In collaboration with Felix Breden, we have investigated opsin photopigments and found polymorphisms in long wavelength opsins between different individuals and populations, indicative of positive selection on red and orange color perception.

Personnel

Dr. Christine Dreyer

Group leader

Dr. Stefan Henz

Staff scientist in bioinformatics

Dr. Margarete Hoffmann

Postdoctoral fellow

Dr. Yuhua Sun

Postdoctoral fellow

Namita Tripathi

Ph.D. student

Dr. Detlef Weigel

Director

Eva-Maria Willing

Ph.D. student

Collaborators

Dr. Paul Bentzen

Dalhousie University, Halifax, Canada

Dr. Felix Breden

Simon Fraser University, British Columbia, Canada

Dr. Joanne Cable

Cardiff University, Cardiff, UK

Dr. Nicolas Langdale

Laboratoire des Interactions Plantes Micro-organismes, Castanet Tolosan, France

Dr. David Reznick

UC Riverside, California, US

Key publications

• Martyn M, Weigel D, Dreyer C. (2006) In vitro culture of embryos of the guppy, Poecilia reticulata. Developmental Dynamics, 235, 605-614.

• Hoffmann M, Tripathi N, Henz SR, Lindholm AK, Weigel D, Breden F, Dreyer C. (2007) Proceedings of the Royal Society B: Biological Sciences, 274, 33-42.
• Dreyer C, Hoffmann M, Lanz C, Willing EM, Riester M, Warthmann N, Sprecher A, Tripathi N, Henz SR, Weigel D. (2007) ESTs and EST-linked polymorphisms for genetic mapping and phylogenetic reconstruction in the guppy, Poecilia reticulata. BMC Genomics 8, 269.

Position open

Ornamental colours of male guppies provide an instructive example of male advantageous traits that are inherited in a sex-linked manner. We have recently established a dense genetic map of the guppy as a major step towards localizing genes involved in quantitative traits, including colour and shape (Tripathi et al, 2008a). Furthermore, we have placed many markers on the sex linkage group of the guppy (Tripathi et al 2008b) and are aiming at identifying the sex determining locus (SDL) on the Y chromosome. The SDL is intimately linked to a number of colour genes, and functional dissection of these loci involves challenging questions about the role of sexually antagonistic genes in the evolution of sex chromosomes.

1. Ph. D. Project : Identity and function of the main sex determining locus (SDL) on the Y-chromosome of the guppy.

The SDL has been mapped to the distal section of the guppy sex linkage group, but its molecular identity remains to be identified. Sex determining mechanisms of teleost fish are diverse, and the SDL may differ even between closely related species. Functional dissection of the guppy SDL and its relationship to the closely linked colour genes will provide further insight in the evolution of sex chromosomes and in the molecular evolution of sex determining genes. The methods include genomic walking using an existing male genomic BAC library, shotgun sequencing by means of modern sequencing techniques, analysis of synteny between species. Sequencing of the transcriptome of Poeciliid fish will enhance further candidate gene approaches in the near future. Applicants should be trained in molecular genetics and be interested in mechanisms of sex determination and evolution of sex chromosomes.

1. Ph. D. Project : How does the adult male colour pattern of guppies emerge?

   What are the mechanisms and time course of specification, migration, multiplication and differentiation of pigment stem cells that originate from embryonic neural crest cells and display their pattern in males after puberty? What is the molecular genetic basis of the heritable patterns and the amazing degree of their natural variation? The methods will comprise cloning of colour genes, analysis of their expression by means of RT-PCR and in situ hybridisation, genetic fine mapping of colour traits as part of genomic analysis. Applicants should be interested in developmental biology and classical as well as molecular genetics.

We offer working in a highly interactive international team involved in research on various aspects of natural variation and evolution.