Statistical method for testing the neutral mutation hypothesis by DNA polymorphism.

In phylogenetic analyses of molecular sequence data, partitioning involves estimating independent models of molecular evolution for different sets of sites in a sequence alignment. Choosing an appropriate partitioning scheme is an important step in most analyses because it can affect the accuracy of phylogenetic reconstruction. Despite this, partitioning schemes are often chosen without explicit statistical justification. Here, we describe two new objective methods for the combined selection of best-fit partitioning schemes and nucleotide substitution models. These methods allow millions of partitioning schemes to be compared in realistic time frames and so permit the objective selection of partitioning schemes even for large multilocus DNA data sets. We demonstrate that these methods significantly outperform previous approaches, including both the ad hoc selection of partitioning schemes (e.g., partitioning by gene or codon position) and a recently proposed hierarchical clustering method. We have implemented these methods in an open-source program, PartitionFinder. This program allows users to select partitioning schemes and substitution models using a range of information-theoretic metrics (e.g., the Bayesian information criterion, akaike information criterion [AIC], and corrected AIC). We hope that PartitionFinder will encourage the objective selection of partitioning schemes and thus lead to improvements in phylogenetic analyses. PartitionFinder is written in Python and runs under Mac OSX 10.4 and above. The program, source code, and a detailed manual are freely available from www.robertlanfear.com/partitionfinder.

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PartitionFinder: Combined Selection of Partitioning Schemes and Substitution Models for Phylogenetic Analyses

Evolution of Protein Molecules

Genetics and analysis of quantitative traits

BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences.

Supergenes are genetic architectures associated with discrete and concerted variation in multiple traits. It has long been suggested that supergenes control these complex polymorphisms by suppressing recombination between sets of coadapted genes. However, because recombination suppression hinders the dissociation of the individual effects of genes within supergenes, there is still little evidence that supergenes evolve by tightening linkage between coadapted genes. Here, combining a landmark-free phenotyping algorithm with multivariate genome-wide association studies, we dissected the genetic basis of wing pattern variation in the butterfly Heliconius numata. We show that the supergene controlling the striking wing pattern polymorphism displayed by this species contains several independent loci associated with different features of wing patterns. The three chromosomal inversions of this supergene suppress recombination between these loci, supporting the hypothesis that they may have evolved because they captured beneficial combinations of alleles. Some of these loci are, however, associated with colour variations only in a subset of morphs where the phenotype is controlled by derived inversion forms, indicating that they were recruited after the formation of the inversions. Our study shows that supergenes and clusters of adaptive loci in general may form via the evolution of chromosomal rearrangements suppressing recombination between co-adapted loci but also via the subsequent recruitment of linked adaptive mutations. This article is part of the theme issue ‘Genomic architecture of supergenes: causes and evolutionary consequences’.

/pdf/association-mapping-of-colour-variation-in-a-butterfly-2lc918j4.pdf

Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci

Identifying the genetic basis of adaptive variation is challenging in non-model organisms and quantitative real time PCR. is a useful tool for validating predictions regarding the expression of candidate genes. However, comparing expression levels in different conditions requires rigorous experimental design and statistical analyses. Here, we focused on the neotropical passion-vine butterflies Heliconius, non-model species studied in evolutionary biology for their adaptive variation in wing color patterns involved in mimicry and in the signaling of their toxicity to predators. We aimed at selecting stable reference genes to be used for normalization of gene expression data in RT-qPCR analyses from developing wing discs according to the minimal guidelines described in Minimum Information for publication of Quantitative Real-Time PCR Experiments (MIQE). To design internal RT-qPCR controls, we studied the stability of expression of nine candidate reference genes (actin, annexin, eF1α, FK506BP, PolyABP, PolyUBQ, RpL3, RPS3A, and tubulin) at two developmental stages (prepupal and pupal) using three widely used programs (GeNorm, NormFinder and BestKeeper). Results showed that, despite differences in statistical methods, genes RpL3, eF1α, polyABP, and annexin were stably expressed in wing discs in late larval and pupal stages of Heliconius numata This combination of genes may be used as a reference for a reliable study of differential expression in wings for instance for genes involved in important phenotypic variation, such as wing color pattern variation. Through this example, we provide general useful technical recommendations as well as relevant statistical strategies for evolutionary biologists aiming to identify candidate-genes involved adaptive variation in non-model organisms.

/pdf/selection-of-valid-reference-genes-for-reverse-transcription-47s34s4g8m.pdf

Selection of Valid Reference Genes for Reverse Transcription Quantitative PCR Analysis in Heliconius numata (Lepidoptera: Nymphalidae).

Sexual interactions play an important role in the evolution of reproductive isolation, with important consequences for speciation. Theoretical studies have focused on the evolution of mate preferences in each sex separately. However, mounting empirical evidence suggests that premating isolation often involves mutual mate choice. Here, using a population genetic model, we investigate how female and male mate choice coevolve under a phenotype matching rule and how this affects reproductive isolation. We show that the evolution of female preferences increases the mating success of males with reciprocal preferences, favouring mutual mate choice. However, the evolution of male preferences weakens indirect selection on female preferences and, with weak genetic drift, the coevolution of female and male mate choice leads to periodic episodes of random mating with increased hybridization (deterministic 'preference cycling' triggered by stochasticity). Thus, counterintuitively, the process of establishing premating isolation proves rather fragile if both male and female mate choice contribute to assortative mating.

/pdf/coevolution-of-male-and-female-mate-choice-can-destabilize-8oz1w2zueq.pdf

Coevolution of male and female mate choice can destabilize reproductive isolation.

The evolution of mate preferences may depend on natural selection acting on the mating cues and on the underlying genetic architecture. While the evolution of assortative mating with respect to locally adapted traits has been well-characterized, the evolution of disassortative mating is poorly characterized. Here we aim at understanding the evolution of disassortative mating for traits under strong balancing selection, by focusing on polymorphic mimicry as an illustrative example. Positive frequency-dependent selection exerted by predators generates local selection on wing patterns acting against rare variants and promoting local monomorphism. This acts across species boundaries, favouring Mullerian mimicry among defended species. In this well-characterized adaptive landscape, polymorphic mimicry is rare but is observed in a butterfly species, associated with polymorphic chromosomal inversions. Because inversions are often associated with recessive deleterious mutations, we hypothesize they may induce heterozygote advantage at the color pattern locus, putatively favoring the evolution of disassortative mating. To explore the conditions underlying the emergence of disassortative mating, we modeled both a trait locus (colour pattern for instance), subject to mutational load, and a preference locus. We confirm that heterozygote advantage favors the evolution of disassortative mating and show that disassortative mating is more likely to emerge if at least one allele at the trait locus is free from any recessive deleterious mutations. We modelled different possible genetic architectures underlying mate choice behaviour, such as self referencing alleles, or specific preference or rejection alleles. Our results showed that self referencing or rejection alleles linked to the color pattern locus can be under positive selection and enable the emergence of disassortative mating. However rejection alleles allow the emergence of disassortative mating only when the color pattern and preference loci are tightly linked. Our results therefore provide relevant predictions on both the selection regimes and the genetic architecture favoring the emergence of disassortative mating and a theoretical framework in which to interprete empirical data on mate preferences in wild populations.

/pdf/evolution-and-genetic-architecture-of-disassortative-mating-1cqsi5jbku.pdf

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

Prey populations have evolved multiple strategies to escape predation. Camouflage is a strategy resting on avoiding detection by potential predators, whereas aposematism relies on advertising chemical defences with conspicuous warning signals. While camouflaged phenotypes are subject to negative frequency-dependent selection, aposematic preys are under positive frequency-dependence, where the efficiency of a signal increases with its own local abundance. Because of his “strength-in-number” effect, multiple chemically-defended species exposed to the same suite of predators gain a selective advantage from converging on the same warning signals. Convergence in warning signals is called Mullerian mimicry. Here, we review the results of recent genetic and ecological research on two well-studied groups of neotropical Mullerian mimetic butterflies, the genus Heliconius and the tribe Ithomiini, which advertise their unpalatability through conspicuous wing colour patterns. Mimicry represents a major adaptation in these groups, where the effects of selection extend well beyond mere phenotypic resemblance. Selection acts on other traits used as mating cues, on the genetic architecture of colour pattern and even on the ecological niche of species. The origin of mimicry itself and the coexistence of multiple mimicry patterns are well understood, but the ultimate drivers of mimicry diversity remain unclear.

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Mathieu Joron

Papers

Association mapping of colour variation in a butterfly provides evidence that a supergene locks together a cluster of adaptive loci

Selection of Valid Reference Genes for Reverse Transcription Quantitative PCR Analysis in Heliconius numata (Lepidoptera: Nymphalidae).

Coevolution of male and female mate choice can destabilize reproductive isolation.

Evolution and genetic architecture of disassortative mating at a locus under heterozygote advantage

Mimicry in Heliconius and Ithomiini butterflies: The profound consequences of an adaptation