@article{concha_wallbank_hanly_fenner_livraghi_rivera_paulo_arias_vargas_sanjeev_et al._2019, title={Interplay between Developmental Flexibility and Determinism in the Evolution of Mimetic Heliconius Wing Patterns}, volume={29}, ISSN={0960-9822}, url={http://dx.doi.org/10.1016/j.cub.2019.10.010}, DOI={10.1016/j.cub.2019.10.010}, abstractNote={To what extent can we predict how evolution occurs? Do genetic architectures and developmental processes canalize the evolution of similar outcomes in a predictable manner? Or do historical contingencies impose alternative pathways to answer the same challenge? Examples of Müllerian mimicry between distantly related butterfly species provide natural replicates of evolution, allowing us to test whether identical wing patterns followed parallel or novel trajectories. Here, we explore the role that the signaling ligand WntA plays in generating mimetic wing patterns in Heliconius butterflies, a group with extraordinary mimicry-related wing pattern diversity. The radiation is relatively young, and numerous cases of wing pattern mimicry have evolved within the last 2.5-4.5 Ma. WntA is an important target of natural selection and is one of four major effect loci that underlie much of the pattern variation in the group. We used CRISPR/Cas9 targeted mutagenesis to generate WntA-deficient wings in 12 species and a further 10 intraspecific variants, including three co-mimetic pairs. In all tested butterflies, WntA knockouts affect pattern broadly and cause a shift among every possible scale cell type. Interestingly, the co-mimics lacking WntA were very different, suggesting that the gene networks that pattern a wing have diverged considerably among different lineages. Thus, although natural selection channeled phenotypic convergence, divergent developmental contexts between the two major Heliconius lineages opened different developmental routes to evolve resemblance. Consequently, even under very deterministic evolutionary scenarios, our results underscore a surprising unpredictability in the developmental paths underlying convergence in a recent radiation.}, number={23}, journal={Current Biology}, publisher={Elsevier BV}, author={Concha, Carolina and Wallbank, Richard W.R. and Hanly, Joseph J. and Fenner, Jennifer and Livraghi, Luca and Rivera, Edgardo Santiago and Paulo, Daniel F. and Arias, Carlos and Vargas, Marta and Sanjeev, Manu and et al.}, year={2019}, month={Dec}, pages={3996–4009.e4} } @article{quek_counterman_moura_cardoso_marshall_mcmillan_kronforst_2010, title={Dissecting comimetic radiations in Heliconius reveals divergent histories of convergent butterflies}, volume={107}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.0911572107}, abstractNote={Mimicry amongHeliconiusbutterflies provides a classic example of coevolution but unresolved relationships among mimetic subspecies have prevented examination of codiversification between species. We present amplified fragment length polymorphism and mtDNA datasets for the major comimetic races ofHeliconius eratoandH. melpomene. The AFLP data reveal unprecedented resolution, clustering samples by geography and race in both species. Our results show that, althoughH. eratoandH. melpomeneco-occur, mimic each other, and exhibit parallel shifts in color pattern, they experienced very different modes of diversification and geographic histories. Our results suggest thatH. eratooriginated on the western side of South America whereasH. melpomeneoriginated in the east.H. eratounderwent rapid diversification and expansion with continued gene-flow following diversification, resulting in widely dispersed sister taxa. In contrast,H. melpomeneunderwent a slower pace of diversification with lower levels of gene flow, producing a stepwise directional expansion from west to east. Our results also suggest that each of the three main wing pattern phenotypes originated and/or was lost multiple times in each species. The rayed pattern is likely to be the ancestral phenotype inH. eratowhereas postman or red patch is likely to be ancestral inH. melpomene. Finally,H. cydnoandH. himeraare monophyletic entities clearly nested withinH. melpomeneandH. erato, rather than being their respective sister species. Estimates of mtDNA divergence suggest a minimum age of 2.8 and 2.1 My forH. eratoandH. melpomene, respectively, placing their origins in the late Pliocene.}, number={16}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Quek, Swee-Peck and Counterman, Brian A. and Moura, Priscila Albuquerque and Cardoso, Marcio Z. and Marshall, Charles R. and McMillan, W. Owen and Kronforst, Marcus R.}, year={2010}, month={Apr}, pages={7365–7370} } @article{counterman_araujo-perez_hines_baxter_morrison_lindstrom_papa_ferguson_joron_ffrench-constant_et al._2010, title={Genomic hotspots for adaptation: The population genetics of Mullerian mimicry in Heliconius erato}, volume={6}, number={4}, journal={PLoS Genetics}, author={Counterman, B. A. and Araujo-Perez, F. and Hines, H. M. and Baxter, S. W. and Morrison, C. M. and Lindstrom, D. P. and Papa, R. and Ferguson, L. and Joron, M. and Ffrench-Constant, R. H. and et al.}, year={2010} } @article{baxter_nadeau_maroja_wilkinson_counterman_dawson_beltran_perez-espona_chamberlain_ferguson_et al._2010, title={Genomic hotspots for adaptation: The population genetics of Mullerian mimicry in the Heliconius melpomene Clade}, volume={6}, number={4}, journal={PLoS Genetics}, author={Baxter, S. W. and Nadeau, N. J. and Maroja, L. S. and Wilkinson, P. and Counterman, B. A. and Dawson, A. and Beltran, M. and Perez-Espona, S. and Chamberlain, N. and Ferguson, L. and et al.}, year={2010} } @article{papa_morrison_walters_counterman_chen_halder_ferguson_chamberlain_ffrench-constant_kapan_et al._2008, title={Highly conserved gene order and numerous novel repetitive elements in genomic regions linked to wing pattern variation in Heliconius butterflies}, volume={9}, ISSN={["1471-2164"]}, DOI={10.1186/1471-2164-9-345}, abstractNote={With over 20 parapatric races differing in their warningly colored wing patterns, the butterfly Heliconius erato provides a fascinating example of an adaptive radiation. Together with matching races of its co-mimic Heliconius melpomene, H. erato also represents a textbook case of Müllerian mimicry, a phenomenon where common warning signals are shared amongst noxious organisms. It is of great interest to identify the specific genes that control the mimetic wing patterns of H. erato and H. melpomene. To this end we have undertaken comparative mapping and targeted genomic sequencing in both species. This paper reports on a comparative analysis of genomic sequences linked to color pattern mimicry genes in Heliconius.Scoring AFLP polymorphisms in H. erato broods allowed us to survey loci at approximately 362 kb intervals across the genome. With this strategy we were able to identify markers tightly linked to two color pattern genes: D and Cr, which were then used to screen H. erato BAC libraries in order to identify clones for sequencing. Gene density across 600 kb of BAC sequences appeared relatively low, although the number of predicted open reading frames was typical for an insect. We focused analyses on the D- and Cr-linked H. erato BAC sequences and on the Yb-linked H. melpomene BAC sequence. A comparative analysis between homologous regions of H. erato (Cr-linked BAC) and H. melpomene (Yb-linked BAC) revealed high levels of sequence conservation and microsynteny between the two species. We found that repeated elements constitute 26% and 20% of BAC sequences from H. erato and H. melpomene respectively. The majority of these repetitive sequences appear to be novel, as they showed no significant similarity to any other available insect sequences. We also observed signs of fine scale conservation of gene order between Heliconius and the moth Bombyx mori, suggesting that lepidopteran genome architecture may be conserved over very long evolutionary time scales.Here we have demonstrated the tractability of progressing from a genetic linkage map to genomic sequence data in Heliconius butterflies. We have also shown that fine-scale gene order is highly conserved between distantly related Heliconius species, and also between Heliconius and B. mori. Together, these findings suggest that genome structure in macrolepidoptera might be very conserved, and show that mapping and positional cloning efforts in different lepidopteran species can be reciprocally informative.}, journal={BMC GENOMICS}, author={Papa, Riccardo and Morrison, Clayton M. and Walters, James R. and Counterman, Brian A. and Chen, Rui and Halder, Georg and Ferguson, Laura and Chamberlain, Nicola and Ffrench-Constant, Richard and Kapan, Durrell D. and et al.}, year={2008}, month={Jul} }