Timing major conflict between mitochondrial and nuclear genes in species relationships of Polygonia butterflies (Nymphalidae: Nymphalini).

Niklas Wahlberg,Sören Nylin,Andrew D Warren,Elisabet Weingartner

doi:10.1186/1471-2148-9-92

Abstract

BackgroundMajor conflict between mitochondrial and nuclear genes in estimating species relationships is an increasingly common finding in animals. Usually this is attributed to incomplete lineage sorting, but recently the possibility has been raised that hybridization is important in generating such phylogenetic patterns. Just how widespread ancient and/or recent hybridization is in animals and how it affects estimates of species relationships is still not well-known.ResultsWe investigate the species relationships and their evolutionary history over time in the genus Polygonia using DNA sequences from two mitochondrial gene regions (COI and ND1, total 1931 bp) and four nuclear gene regions (EF-1α, wingless, GAPDH and RpS5, total 2948 bp). We found clear, strongly supported conflict between mitochondrial and nuclear DNA sequences in estimating species relationships in the genus Polygonia. Nodes at which there was no conflict tended to have diverged at the same time when analyzed separately, while nodes at which conflict was present diverged at different times. We find that two species create most of the conflict, and attribute the conflict found in Polygonia satyrus to ancient hybridization and conflict found in Polygonia oreas to recent or ongoing hybridization. In both examples, the nuclear gene regions tended to give the phylogenetic relationships of the species supported by morphology and biology.ConclusionStudies inferring species-level relationships using molecular data should never be based on a single locus. Here we show that the phylogenetic hypothesis generated using mitochondrial DNA gives a very different interpretation of the evolutionary history of Polygonia species compared to that generated from nuclear DNA. We show that possible cases of hybridization in Polygonia are not limited to sister species, but may be inferred further back in time. Furthermore, we provide more evidence that Haldane's effect might not be as strong a process in preventing hybridization in butterflies as has been previously thought.

Highlights

Major conflict between mitochondrial and nuclear genes in estimating species relationships is an increasingly common finding in animals
Most species-level phylogenies have until recently been based on only mitochondrial DNA due to the ease of PCR amplification and its perceived suitability, e.g. due to maternal inheritance (shorter time for coalescence than nuclear DNA because of smaller Ne), lack of recombination and relatively high mutation rate
The genus Polygonia without the species Kaniska canace is strongly supported by all datasets

Summary

Introduction

Major conflict between mitochondrial and nuclear genes in estimating species relationships is an increasingly common finding in animals This is attributed to incomplete lineage sorting, but recently the possibility has been raised that hybridization is important in generating such phylogenetic patterns. Genes involved with speciation, affecting such traits as hybrid incompatibility, as well as sex chromosomes should be more differentiated between species and less likely to introgress than autosomes [5,6,7,8]. Different processes such as random sorting of homoplasy, ancient polymorphism and hybridization with gene introgression can obscure patterns of species relationships. Information from different regions of genomes such as mitochondrial DNA, nuclear DNA (from sex chromosomes as well as from autosomes) and microsatellites are necessary in investigating the evolutionary history of a group of closely related species

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