Wing Patterns in the Mist

Perspective Wing Patterns in the Mist Arnaud Martin 1 , Durrell D. Kapan 2 , Lawrence E. Gilbert 3 * 1 Ecology and Evolutionary Biology, School of Biological Sciences, University of California Irvine, Irvine, California, United States of America, 2 Center for Conservation and Research Training, Pacific Biosciences Research Center, University of Hawaii at Manoa, Honolulu, Hawaii, United States of America, 3 Section of Integrative Biology, School of Biological Sciences and Brackenridge Field Laboratory, University of Texas at Austin, Austin, Texas, United States of America The aesthetic appeal of butterfly wing patterns has been costly to their status as a tool of fundamental scientific inquiry. Thus, while mimetic convergence in wing patterns between edible ‘‘Batesian’’ mim- ics and distasteful models, or between different distasteful ‘‘Mu¨llerian’’ mimics (species that cooperate to educate preda- tors) has long been the subject of genetic analysis [1] and field experiments [2], most biology text books confine mimicry to sections on striking adaptations without applying these examples to broader topics of evolution. Meanwhile, the study of color patterns in animals, often tucked into the same sections of texts, is undergoing a revolution in this age of evo-devo and genomics [3]. Among insect models for studying color pattern, the genus Heliconius is gaining the attention of an ever- widening audience ([4–6]; Figure 1). Heliconius : Taxonomic Hotspot Early in the 20th century, Oxford’s pre-eminent evolutionist and student of insect color patterns, Edward B. Poulton, urged Harry Eltringham to study taxo- nomic relationships of a spectacularly colorful, mimetic, and diverse set of specimens pouring into European muse- ums from field collectors across the Neotropics. Eltringham [7] distinguished Heliconius erato and Heliconius melpomene groupings and noted repeated mimetic convergence between them. However, within those groupings, he failed to distinguish species, races, and hybrids. In the mid 1950s, William Beebe and associates initiated studies of life history, behavior, systematics, and genetics of Heliconius at Simla in Trinidad. There, Michael Emsley elucidated biogeographic details of the system [8]. It soon became clear that many rare ‘‘taxa’’ described as species by museum workers were in fact recombinants occurring in narrow hybrid zones between two distinct mimetic races. In these zones Mu¨llerian partners erato and melpomene each generate similar arrays of hybrid phenotypes, many of which would be sufficiently distinct to warrant separate species status when viewed out of context. PLoS Genetics | www.plosgenetics.org Genetics of Parallel Mimetic Radiations In the 1960s, genetic studies of H. erato and H. melpomene at Simla established the framework of classification of pattern loci in general use today [9]. In 1979, Turner [10] reported a strong discrepancy in levels of differentiation in color pattern versus allozyme loci across the geograph- ical range of erato and melpomene. Thus, if viewed only through the lens of structural genes not manifest in the visible pheno- type, few of the many races described for these species would be delimited. Later research in Peru on selection and gene flow in parallel interracial hybrid zones by James Mallet [11] set the stage for work on genomic hot spots described in this issue Several teams have been busy in recent years trying to relate underlying allelic variation in color pattern observed in laboratory crosses and in natural hybrid zones to changes occurring in the ge- nome. Classic genetic mapping previously showed that these adaptive polymor- phisms in four different radiations were linked to homologous intervals [14–16]. In particular, the B/D locus, which controls the presence/absence of red patterns, and the Yb/Cr locus, which controls the presence/absence of a yellow bar, respectively map to homologous linkage groups between the co-mimics H. melpomene and H. erato, although co- mimetic phenotypes evolved indepen- dently. In other words, convergent evolu- tion in wing patterning between species involved the same genetic intervals, and, since synteny between distantly related Lepidoptera is conserved [17], by exten- sion, likely many of the same genes. This ignited a push to narrow the search to actual genes or nucleotide changes re- sponsible for parallel wing pattern shifts, to illuminate genetic and developmental mechanisms responsible for generating spectacular and adaptive morphological diversity. Are cis-regulatory or trans-regu- latory changes responsible for these poly- morphisms [18,19]? Do similar pheno- types reflect identical nucleotide changes, or independent functional changes in homologous genes or developmental pathways? The current work appears to be on a path that will help resolve questions about genotype phenotype con- nections. Hybrid Zones Uncover the Smoking Guns of Selection The Heliconius system forms a unique replicated natural experiment to study the genetics of adaptive traits: allowing com- parison between parapatric races of different phenotypes, between geograph- ically distant races of similar phenotypes, and finally, between different species (co- mimics) across parallel inter-racial hybrid zones. The papers in this issue exploit this system by seeking signatures of selection across previously identified genetic inter- vals B/D and Yb/Cr in hybrid zones where populations of different phenotypes are admixed. Indeed, in these species mimicry ring structure on both sides of a hybrid zone imposes a strong positive frequent-dependent selection favoring common wing patterns [2,11]. This is expected to result in a peak of population differentiation at causative genetic loci, because pattern alleles from race A that Citation: Martin A, Kapan DD, Gilbert LE (2010) Wing Patterns in the Mist. PLoS Genet 6(2): e1000822. doi:10.1371/journal.pgen.1000822 Editor: Michael W. Nachman, University of Arizona, United States of America Published February 5, 2010 Copyright: s 2010 Martin et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors received no specific funding for this article. Competing Interests: The authors have declared that no competing interests exist. * E-mail: lgilbert@mail.utexas.edu February 2010 | Volume 6 | Issue 2 | e1000822