Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data

Beltrán, Margarita; Jiggins, Chris D.; Brower, Andrew V. Z.; Bermingham, Eldredge; Mallet, James

doi:10.1111/j.1095-8312.2007.00830.x

Cited by 151 publications

(210 citation statements)

References 66 publications

(116 reference statements)

Supporting

Mentioning

197

Contrasting

Order By: Relevance

“…Furthermore, although patterns are not transferred between H. erato and H. melpomene, H. melpomene may have acquired different red pattern phenotypes through hybridization with its closest relatives. H. melpomene is a member of a larger complex of species that are known to hybridize in nature, including a number of species in the Amazon region with rayed phenotypes (1,27). The acquisition of new color patterns by hybridization is thought to play an important role in the evolution of pattern variation in Heliconius (24,28,29).…”

Section: Discussionmentioning

confidence: 99%

Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Hines

Counterman

Papa

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

115

172

View full text Add to dashboard Cite

The mimetic butterflies Heliconius erato and Heliconius melpomene have undergone parallel radiations to form a near-identical patchwork of over 20 different wing-pattern races across the Neotropics. Previous molecular phylogenetic work on these radiations has suggested that similar but geographically disjunct color patterns arose multiple times independently in each species. The neutral markers used in these studies, however, can move freely across color pattern boundaries, and therefore might not represent the history of the adaptive traits as accurately as markers linked to color pattern genes. To assess the evolutionary histories across different loci, we compared relationships among races within H. erato and within H. melpomene using a series of unlinked genes, genes linked to color pattern loci, and optix, a gene recently shown to control red colorpattern variation. We found that although unlinked genes partition populations by geographic region, optix had a different history, structuring lineages by red color patterns and supporting a single origin of red-rayed patterns within each species. Genes closely linked (80-250 kb) to optix exhibited only weak associations with color pattern. This study empirically demonstrates the necessity of examining phenotype-determining genomic regions to understand the history of adaptive change in rapidly radiating lineages. With these refined relationships, we resolve a long-standing debate about the origins of the races within each species, supporting the hypothesis that the red-rayed Amazonian pattern evolved recently and expanded, causing disjunctions of more ancestral patterns.Müllerian mimicry | population genetics | phylogeography R esearchers typically rely on neutrally evolving loci to generate a phylogenetic and population genetic history of adaptive divergence. The rationale is that these markers provide an unbiased view of the relationships among divergent phenotypes and a better understanding of the evolutionary processes generating variation. However, the genome is a complicated mosaic shaped by an interplay of mutation, drift, selection, and recombination. Recombination allows different regions of the genome to experience alternative restrictions to gene flow, and thus develop different evolutionary trajectories. The closer a genetic marker is to the alleles responsible for adaptive differences, the more likely that it will trace the history of phenotypic change.Understanding how phenotypic variation is generated in nature is greatly enhanced by studying groups that are actively undergoing diversification. By deciphering the history of such diverse phenotypes we gain a clearer understanding of the evolutionary process, including the tempo and mode of phenotypic change. Heliconius butterflies present one of the most striking examples of a recent phenotypic radiation. The 40 species in the genus exhibit hundreds of wing patterns that are involved in Müllerian mimicry complexes, where distasteful species converge on a shared warning signal to avoid predation. Th...

show abstract

Section: Discussionmentioning

confidence: 99%

Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Hines

Counterman

Papa

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

115

172

View full text Add to dashboard Cite

show abstract

“…These disadvantages of relying solely on mtDNA genes mean that studies using multigene phylogenies integrating information from both nuclear and mitochondrial sequences are becoming more prevalent in plants and animals (Beltrán et al, 2007;Alfaro et al, 2008;Hugall et al, 2008). Relatively fast evolving sequences are required to determine species-level relationships, and nuclear coding regions are preferable as frequent indels in non-coding regions create length polymorphism requiring post-PCR cloning before sequencing.…”

Section: Introductionmentioning

confidence: 99%

Pinniped phylogenetic relationships inferred using AFLP markers

2009

View full text Add to dashboard Cite

Amplified fragment length polymorphisms (AFLPs) are widely used for phylogenetic reconstruction in plants but their use in animal taxa has been limited, and in mammals rare. In addition, their use has been largely limited to shallow relationships amongst species or subspecies. Here, we genotype 23 pinniped species for 310 AFLP markers and find a strong phylogenetic signal, with individuals coclustering within species, and overall a good agreement between our phylogeny and those constructed using mitochondrial DNA and nuclear sequences even at nodes B15 million years old. Although supporting the existing ideas about pinniped relationships, our data shed light on relationships within the hitherto relatively unresolved Phocine species group, and provide further supporting evidence for raising two subspecies of Zalophus californianus, Z. c. californianus and Z. c. wollebaeki, to species level. Plotting AFLP divergence time estimates against those based on both mtDNA and nuclear sequences we find strong linear relationships, suggesting that the different markers are evolving in a clocklike fashion. These data further emphasize the utility of AFLP markers as general tools for phylogenetic reconstruction.

show abstract

“…Heliconiini systematics has a long history, starting with early morphological work (Emsley 1965;Brown 1981;Penz 1999), through allozymes (Turner et al 1979) and a combination of morphological and ribosomal DNA-restriction data (Lee et al 1992), to studies based on the sequences of mitochondrial and nuclear markers (Brower 1994b;Brower and Egan 1997;Beltrán et al 2002Beltrán et al , 2007Cuthill and Charleston 2012;Massardo et al 2014). The most comprehensive study to date by Beltrán et al (2007) attempted to address some of the difficulties by incorporating many taxa (38 of 46 Heliconius, 59 of 77 Heliconiini), considering two individuals of most species, and sequencing two mitochondrial (CoI/II and 16S) and four nuclear markers (EF1, Wg, Ap, and Dpp).…”

mentioning

confidence: 99%

“…The most comprehensive study to date by Beltrán et al (2007) attempted to address some of the difficulties by incorporating many taxa (38 of 46 Heliconius, 59 of 77 Heliconiini), considering two individuals of most species, and sequencing two mitochondrial (CoI/II and 16S) and four nuclear markers (EF1, Wg, Ap, and Dpp). However, this data set is still potentially inadequate to address the challenges posed by Heliconiini systematics, as 3 of the loci (16S, Ap, and Dpp) were only sequenced for 12 representative species.…”

mentioning

confidence: 99%

Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies

Kozak

Wahlberg

Neild

et al. 2014

Preprint

Self Cite

129

View full text Add to dashboard Cite

Abstract.-Müllerian mimicry among Neotropical Heliconiini butterflies is an excellent example of natural selection, associated with the diversification of a large continental-scale radiation. Some of the processes driving the evolution of mimicry rings are likely to generate incongruent phylogenetic signals across the assemblage, and thus pose a challenge for systematics. We use a data set of 22 mitochondrial and nuclear markers from 92% of species in the tribe, obtained by Sanger sequencing and de novo assembly of short read data, to re-examine the phylogeny of Heliconiini with both supermatrix and multispecies coalescent approaches, characterize the patterns of conflicting signal, and compare the performance of various methodological approaches to reflect the heterogeneity across the data. Despite the large extent of reticulate signal and strong conflict between markers, nearly identical topologies are consistently recovered by most of the analyses, although the supermatrix approach failed to reflect the underlying variation in the history of individual loci. However, the supermatrix represents a useful approximation where multiple rare species represented by short sequences can be incorporated easily. The first comprehensive, time-calibrated phylogeny of this group is used to test the hypotheses of a diversification rate increase driven by the dramatic environmental changes in the Neotropics over the past 23 myr, or changes caused by diversity-dependent effects on the rate of diversification. We find that the rate of diversification has increased on the branch leading to the presently most species-rich genus Heliconius, but the change occurred gradually and cannot be unequivocally attributed to a specific environmental driver. Our study provides comprehensive comparison of philosophically distinct species tree reconstruction methods and provides insights into the diversification of an important insect radiation in the most biodiverse region of the planet.

show abstract

Do pollen feeding, pupal-mating and larval gregariousness have a single origin in Heliconius butterflies? Inferences from multilocus DNA sequence data

Cited by 151 publications

References 66 publications

Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Wing patterning gene redefines the mimetic history ofHeliconiusbutterflies

Pinniped phylogenetic relationships inferred using AFLP markers

Multilocus Species Trees Show the Recent Adaptive Radiation of the Mimetic Heliconius Butterflies

Contact Info

Product

Resources

About