Comparative mitochondrial genomics within and among species of killifish

Andrew Whitehead

doi:10.1186/1471-2148-9-11

Abstract

BackgroundThis study was motivated by the observation of unusual mitochondrial haplotype distributions and associated physiological differences between populations of the killifish Fundulus heteroclitus distributed along the Atlantic coast of North America. A distinct "northern" haplotype is fixed in all populations north of New Jersey, and does not appear south of New Jersey except in extreme upper-estuary fresh water habitats, and northern individuals are known to be more tolerant of hyposmotic conditions than southern individuals. Complete mitochondrial genomes were sequenced from individuals from northern coastal, southern coastal, and fresh water populations (and from out-groups). Comparative genomics approaches were used to test multiple evolutionary hypotheses proposed to explain among-population genome variation including directional selection and hybridization.ResultsStructure and organization of the Fundulus mitochondrial genome is typical of animals, yet subtle differences in substitution patterns exist among populations. No signals of directional selection or hybridization were detected. Mitochondrial genes evolve at variable rates, but all genes exhibit very low dN/dS ratios across all lineages, and the southern population harbors more synonymous polymorphism than other populations.ConclusionEvolution of mitochondrial genomes within Fundulus is primarily governed by interaction between strong purifying selection and demographic influences, including larger historical population size in the south. Though directional selection and hybridization hypotheses were not supported, adaptive processes may indirectly contribute to partitioning of variation between populations.

Highlights

This study was motivated by the observation of unusual mitochondrial haplotype distributions and associated physiological differences between populations of the killifish Fundulus heteroclitus distributed along the Atlantic coast of North America
Phylogenetic analyses were used to test for possible hybridization between F. diaphanus and co-occurring F. heteroclitus populations. These analyses examined the relationship of Fundulus populations and species (Acanthopterygii; Atherinomorpha; Cyprinodontiformes; Fundulidae) to each other and to other closely related fishes for which complete mitogenomes exist including Cyprinodon rubrofluviatilis (Acanthopterygii; Atherinomorpha; Cyprinodontiformes; Cyprinodontidae), Gambusia affinis (Acanthopterygii; Atherinomorpha; Cyprinodontiformes; Poeciliidae), Kryptolebias marmoratus (Acanthopterygii; Atherinomorpha; Cyprinodontiformes; Rivulidae), Oryzias latipes (Acanthopterygii; Atherinomorpha; Beloniformes), Cololabis saira
Broader analysis of all complete mitochondrial genomes that are currently available for the clade indicate that cyprinodontiformes and beloniformes fishes are reciprocally monophyletic (Figure 1), in contrast to the findings reported in Miya et al [52]

Summary

Introduction

Fundulus heteroclitus is a euryhaline killifish that occupies diverse habitats along steep osmotic and thermal gradients; large populations are found in extreme upper-estuary fresh water sites through brackish estuarine habitats to marine environments, and across a steep latitudinal temperature gradient along the Atlantic coast of North America from Nova Scotia (Canada) to Florida (USA). This species has long been of interest to science in part because of their extraordinary physiological resilience in the face of osmotic stress [1], and as a model for studying adaptive evolutionary variation along ecological clines [2]. The purpose of this study was to compare mitochondrial genome variation within and among Fundulus species to test this and related hypotheses

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Conclusion