@article{paulo_junqueira_arp_vieira_ceballos_skoda_pérez-de-león_sagel_mcmillan_scott_et al._2021, title={Disruption of the odorant coreceptor Orco impairs foraging and host finding behaviors in the New World screwworm fly}, volume={11}, ISSN={2045-2322}, url={http://dx.doi.org/10.1038/s41598-021-90649-x}, DOI={10.1038/s41598-021-90649-x}, abstractNote={AbstractThe evolution of obligate ectoparasitism in blowflies (Diptera: Calliphoridae) has intrigued scientists for over a century, and surprisingly, the genetics underlying this lifestyle remain largely unknown. Blowflies use odors to locate food and oviposition sites; therefore, olfaction might have played a central role in niche specialization within the group. In insects, the coreceptor Orco is a required partner for all odorant receptors (ORs), a major gene family involved in olfactory-evoked behaviors. Hence, we characterized the Orco gene in the New World screwworm, Cochliomyia hominivorax, a blowfly that is an obligate ectoparasite of warm-blooded animals. In contrast, most of the closely related blowflies are scavengers that lay their eggs on dead animals. We show that the screwworm Orco orthologue (ChomOrco) is highly conserved within Diptera, showing signals of strong purifying selection. Expression of ChomOrco is broadly detectable in chemosensory appendages, and is related to morphological, developmental, and behavioral aspects of the screwworm biology. We used CRISPR/Cas9 to disrupt ChomOrco and evaluate the consequences of losing the OR function on screwworm behavior. In two-choice assays, Orco mutants displayed an impaired response to floral-like and animal host-associated odors, suggesting that OR-mediated olfaction is involved in foraging and host-seeking behaviors in C. hominivorax. These results broaden our understanding of the chemoreception basis of niche occupancy by blowflies.}, number={1}, journal={Scientific Reports}, publisher={Springer Science and Business Media LLC}, author={Paulo, Daniel F. and Junqueira, Ana C. M. and Arp, Alex P. and Vieira, André S. and Ceballos, Jorge and Skoda, Steven R. and Pérez-de-León, Adalberto A. and Sagel, Agustin and McMillan, William O. and Scott, Maxwell J. and et al.}, year={2021}, month={May} }
 @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{hines_counterman_papa_moura_cardoso_linares_mallet_reed_jiggins_kronforst_et al._2011, title={Wing patterning gene redefines the mimetic history of Heliconius butterflies}, volume={108}, ISSN={["0027-8424"]}, DOI={10.1073/pnas.1110096108}, abstractNote={The mimetic butterfliesHeliconius eratoandHeliconius melpomenehave 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 withinH. eratoand withinH. melpomeneusing a series of unlinked genes, genes linked to color pattern loci, andoptix, a gene recently shown to control red color-pattern variation. We found that although unlinked genes partition populations by geographic region,optixhad 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) tooptixexhibited 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.}, number={49}, journal={PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA}, author={Hines, Heather M. and Counterman, Brian A. and Papa, Riccardo and Moura, Priscila Albuquerque and Cardoso, Marcio Z. and Linares, Mauricio and Mallet, James and Reed, Robert D. and Jiggins, Chris D. and Kronforst, Marcus R. and et al.}, year={2011}, month={Dec}, pages={19666–19671} }
 @article{reed_papa_martin_hines_counterman_pardo-diaz_jiggins_chamberlain_kronforst_chen_et al._2011, title={optix Drives the Repeated Convergent Evolution of Butterfly Wing Pattern Mimicry}, volume={333}, ISSN={["1095-9203"]}, DOI={10.1126/science.1208227}, abstractNote={
            Heliconius
            butterfly wing pattern mimicry is driven by cis-regulatory variation of the
            optix
            gene.
          }, number={6046}, journal={SCIENCE}, author={Reed, Robert D. and Papa, Riccardo and Martin, Arnaud and Hines, Heather M. and Counterman, Brian A. and Pardo-Diaz, Carolina and Jiggins, Chris D. and Chamberlain, Nicola L. and Kronforst, Marcus R. and Chen, Rui and et al.}, year={2011}, month={Aug}, pages={1137–1141} }
 @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{ceron-souza_rivera-ocasio_medina_jimenez_mcmillan_bermingham_2010, title={HYBRIDIZATION AND INTROGRESSION IN NEW WORLD RED MANGROVES, RHIZOPHORA (RHIZOPHORACEAE)}, volume={97}, ISSN={["1537-2197"]}, DOI={10.3732/ajb.0900172}, abstractNote={•Premise of the study:Hybridization is common in both animals and plants and can lead to a diverse array of outcomes ranging from the generation of new ecotypes or species to the breakdown of morphological differences. Here, we explore the extent of hybridization in the three currently recognized New WorldRhizophoraspecies—R. mangle, R. racemosa, and the putative hybrid speciesR. harrisonii.•Methods:We assayed variation across the three recognizedRhizophoraspecies using two noncoding chloroplast (cpDNA), two flanking microsatellite regions (FMRs), and six microsatellite loci.•Key results:Gene genealogies of cpDNA and FMRs showed a strong phylogeographic break across the Central American Isthmus, but little relationship to recognized species boundaries. Instead, individuals collected in the same ocean basin and classified asR. mangleandR. racemosaby morphological characteristics were more closely related to each other than with similar looking individuals collected in the other ocean basin. Nonetheless, there were low, yet significant differences at microsatellite loci among co‐occurring populations ofR. mangleandR. racemosain both ocean basins, suggesting that two taxonomic groups coexist. However, we found no genetic evidence thatR. harrisoniiwas a hybrid species. Rather,R. harrisoniiappears to represent a morphotype produced by ongoing hybridization and backcrossing betweenR. mangleandR. racemosa.•Conclusions:Our data support ancient and persistent introgressive hybridization among new worldRhizophoraand argue for a full revision of the systematic relationships of the group based on much finer morphological, ecological, and genetic analyses.}, number={6}, journal={AMERICAN JOURNAL OF BOTANY}, author={Ceron-Souza, Ivania and Rivera-Ocasio, Elsie and Medina, Ernesto and Jimenez, Jorge A. and McMillan, W. Owen and Bermingham, Eldredge}, year={2010}, month={Jun}, pages={945–957} }
 @article{merrill_gompert_dembeck_kronforst_mcmillan_jiggins_2011, title={MATE PREFERENCE ACROSS THE SPECIATION CONTINUUM IN A CLADE OF MIMETIC BUTTERFLIES}, volume={65}, ISSN={["1558-5646"]}, DOI={10.1111/j.1558-5646.2010.01216.x}, abstractNote={Premating behavioral isolation is increasingly recognized as an important part of ecological speciation, where divergent natural selection causes the evolution of reproductive barriers. A number of studies have now demonstrated that traits under divergent natural selection also affect mate preferences. However, studies of single species pairs only capture a snapshot of the speciation process, making it difficult to assess the role of mate preferences throughout the entire process. Heliconius butterflies are well known for their brightly colored mimetic warning patterns, and previous studies have shown that these patterns are also used as mate recognition cues. Here, we present mate preference data for four pairs of sister taxa, representing different stages of divergence, which together allow us to compare diverging mate preferences across the continuum of Heliconius speciation. Using a novel Bayesian approach, our results support a model of ecological speciation in which strong premating isolation arises early, but continues to increase throughout the continuum from polymorphic populations through to “good,” sympatric ecologically divergent species.}, number={5}, journal={EVOLUTION}, author={Merrill, Richard M. and Gompert, Zachariah and Dembeck, Lauren M. and Kronforst, Marcus R. and McMillan, W. Owen and Jiggins, Chris D.}, year={2011}, month={May}, pages={1489–1500} }
 @article{baxter_papa_chamberlain_humphray_joron_morrison_ffrench-constant_mcmillan_jiggins_2008, title={Convergent Evolution in the Genetic Basis of Mullerian Mimicry in Heliconius Butterflies}, volume={180}, ISSN={["1943-2631"]}, DOI={10.1534/genetics.107.082982}, abstractNote={AbstractThe neotropical butterflies Heliconius melpomene and H. erato are Müllerian mimics that display the same warningly colored wing patterns in local populations, yet pattern diversity between geographic regions. Linkage mapping has previously shown convergent red wing phenotypes in these species are controlled by loci on homologous chromosomes. Here, AFLP bulk segregant analysis using H. melpomene crosses identified genetic markers tightly linked to two red wing-patterning loci. These markers were used to screen a H. melpomene BAC library and a tile path was assembled spanning one locus completely and part of the second. Concurrently, a similar strategy was used to identify a BAC clone tightly linked to the locus controlling the mimetic red wing phenotypes in H. erato. A methionine rich storage protein (MRSP) gene was identified within this BAC clone, and comparative genetic mapping shows red wing color loci are in homologous regions of the genome of H. erato and H. melpomene. Subtle differences in these convergent phenotypes imply they evolved independently using somewhat different developmental routes, but are nonetheless regulated by the same switch locus. Genetic mapping of MRSP in a third related species, the “tiger” patterned H. numata, has no association with wing patterning and shows no evidence for genomic translocation of wing-patterning loci.}, number={3}, journal={GENETICS}, author={Baxter, Simon W. and Papa, Riccardo and Chamberlain, Nicola and Humphray, Sean J. and Joron, Mathieu and Morrison, Clay and Ffrench-Constant, Richard H. and McMillan, W. Owen and Jiggins, Chris D.}, year={2008}, month={Nov}, pages={1567–1577} }
 @article{velez-zuazo_ramos_dam_diez_abreu-grobois_mcmillan_2008, title={Dispersal, recruitment and migratory behaviour in a hawksbill sea turtle aggregation}, volume={17}, ISSN={["1365-294X"]}, DOI={10.1111/j.1365-294X.2007.03635.x}, abstractNote={AbstractWe investigated the dispersal, recruitment and migratory behaviour of the hawksbill sea turtle (Eretmochelys imbricata), among different life‐history stages and demographic segments of the large hawksbill turtle aggregation at Mona Island, Puerto Rico. There were significant differences in both mitochondrial DNA (mtDNA) haplotype diversity and haplotype frequencies among the adult males, females and juveniles examined, but little evidence for temporal heterogeneity within these same groups sampled across years. Consistent with previous studies and the hypothesis of strong natal homing, there were striking mtDNA haplotype differences between nesting females on Mona Island and nesting females in other major Caribbean rookeries. Breeding males also showed strong, albeit weaker, genetic evidence of natal homing. Overall, Bayesian mixed‐stock analysis suggests that Mona Island was the natal rookery for 79% (65–94%) of males in the aggregation. In contrast, the Mona Island rookery accounted for only a small subset of the new juvenile recruits to the foraging grounds or in the population of older juvenile hawksbills turtles on Mona. Instead, both new recruits and the older juvenile hawksbill turtles on Mona more likely recruited from other Caribbean rookeries, suggesting that a mechanism besides natal homing must be influencing recruitment to feeding habitats. The difference in the apparent degree of natal homing behaviour among the different life‐history stages of hawksbill turtles at Mona Island underscores the complexity of the species’ life‐history dynamics and highlights the need for both local and regional conservation efforts.}, number={3}, journal={MOLECULAR ECOLOGY}, author={Velez-Zuazo, Ximena and Ramos, Willy D. and Dam, Robert P. and Diez, Carlos E. and Abreu-Grobois, Alberto and Mcmillan, W. Owen}, year={2008}, month={Feb}, pages={839–853} }
 @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} }
 @article{papanicolaou_gebauer-jung_blaxter_mcmillan_jiggins_2008, title={ButterflyBase: a platform for lepidopteran genomics}, volume={36}, ISSN={["1362-4962"]}, DOI={10.1093/nar/gkm853}, abstractNote={With over 100 000 species and a large community of evolutionary biologists, population ecologists, pest biologists and genome researchers, the Lepidoptera are an important insect group. Genomic resources [expressed sequence tags (ESTs), genome sequence, genetic and physical maps, proteomic and microarray datasets] are growing, but there has up to now been no single access and analysis portal for this group. Here we present ButterflyBase (http://www.butterflybase.org), a unified resource for lepidopteran genomics. A total of 273 077 ESTs from more than 30 different species have been clustered to generate stable unigene sets, and robust protein translations derived from each unigene cluster. Clusters and their protein translations are annotated with BLAST-based similarity, gene ontology (GO), enzyme classification (EC) and Kyoto encyclopaedia of genes and genomes (KEGG) terms, and are also searchable using similarity tools such as BLAST and MS-BLAST. The database supports many needs of the lepidopteran research community, including molecular marker development, orthologue prediction for deep phylogenetics, and detection of rapidly evolving proteins likely involved in host–pathogen or other evolutionary processes. ButterflyBase is expanding to include additional genomic sequence, ecological and mapping data for key species.}, journal={NUCLEIC ACIDS RESEARCH}, author={Papanicolaou, Alexie and Gebauer-Jung, Steffi and Blaxter, Mark L. and McMillan, W. Owen and Jiggins, Chris D.}, year={2008}, month={Jan}, pages={D582–D587} }