Lawrence E. Gilbert

Butterfly genome reveals promiscuous exchange of mimicry adaptations among species

The evolutionary importance of hybridization and introgression has long been debated. Hybrids are usually rare and unfit, but even infrequent hybridization can aid adaptation by transferring beneficial traits between species. Here we use genomic tools to investigate introgression in Heliconius, a rapidly radiating genus of neotropical butterflies widely used in studies of ecology, behaviour, mimicry and speciation. We sequenced the genome of Heliconius melpomene and compared it with other taxa to investigate chromosomal evolution in Lepidoptera and gene flow among multiple Heliconius species and races. Among 12,669 predicted genes, biologically important expansions of families of chemosensory and Hox genes are particularly noteworthy. Chromosomal organization has remained broadly conserved since the Cretaceous period, when butterflies split from the Bombyx (silkmoth) lineage. Using genomic resequencing, we show hybrid exchange of genes between three co-mimics, Heliconius melpomene, Heliconius timareta and Heliconius elevatus, especially at two genomic regions that control mimicry pattern. We infer that closely related Heliconius species exchange protective colour-pattern genes promiscuously, implying that hybridization has an important role in adaptive radiation.

Ovarian Dynamics in Heliconiine Butterflies: Programmed Senescence versus Eternal Youth.

New oocytes are generated throughout long lives in butterflies of the genus Heliconius, which as adults feed on amino acids from pollen. In Dryas julia, a related heliconiine that feeds only on nectar and is relatively short-lived, the original oocyte supply is eventually depleted. Such divergent ovarian dynamics in closely related organisms are significant in terms of both their evolutionary basis and their physiological controls.

Butterfly-Plant Coevolution: Has Passiflora adenopoda Won the Selectional Race with Heliconiine Butterflies?

Hooklike trichomes of Passiflora adenopoda provide a specific, effectively absolute defense against heliconiine butterfly larvae, a major class of Passiflora herbivores. It is suggested that since mechanical defenses are usually more selective in their action against herbivores, they usually are evolved by a plant only after it has accumulated a series of chemical defenses.

MULTILOCUS ANALYSES OF ADMIXTURE AND INTROGRESSION AMONG HYBRIDIZING HELICONIUS BUTTERFLIES

Abstract Introgressive hybridization is an important evolutionary process and new analytical methods provide substantial power to detect and quantify it. In this study we use variation in the frequency of 657 AFLP fragments and DNA sequence variation from 15 genes to measure the extent of admixture and the direction of interspecific gene flow among three Heliconius butterfly species that diverged recently as a result of natural selection for Müllerian mimicry, and which continue to hybridize. Bayesian clustering based on AFLP genotypes correctly delineated the three species and identified four H. cydno, three H. pachinus, and three H. melpomene individuals that were of mixed ancestry. Gene genealogies revealed substantial shared DNA sequence variation among all three species and coalescent simulations based on the Isolation with Migration (IM) model pointed to interspecific gene flow as its cause. The IM simulations further indicated that interspecific gene flow was significantly asymmetrical, with greater gene flow from H. pachinus into H. cydno (2Nm 5 4.326) than the reverse (2Nm 5 0.502), and unidirectional gene flow from H. cydno and H. pachinus into H. melpomene (2Nm 5 0.294 and 0.252, respectively). These asymmetries are in the directions expected based on the genetics of wing patterning and the probability that hybrids of various phenotypes will survive and reproduce in different mimetic environments. This empirical demonstration of extensive interspecific gene flow is in contrast to a previous study which found little evidence of gene flow between another pair of hybridizing Heliconius species, H. himera and H. erato, and it highlights the critical role of natural selection in maintaining species diversity. Furthermore, these results lend support to the hypotheses that phenotypic diversification in the genus Heliconius has been fueled by introgressive hybridization and that reinforcement has driven the evolution of assortative mate preferences.

Polymorphic butterfly reveals the missing link in ecological speciation.

Butterfly Apartheid Heliconius butterflies show differences in mimetic color patterns across geographic races associated with patterns of assortative mating, suggesting that ecological speciation may be ongoing. Chamberlain et al. (p. 847) demonstrate assortative mating on the basis of color pattern mimicry that generates reproductive isolation between Heliconius cydno species and subspecies within polymorphic populations in Ecuador. Furthermore, it appears that these traits are controlled by a single gene that affects color pigment in wing pattern formation and vision. Thus, these butterflies are indeed in the early stages of reproductive isolation that is being driven by an ecological trait, allowing observation of an incipient speciation event. Mate selection based on preferences for polymorphic wing color patterns is generating reproductive isolation. Ecological speciation occurs when ecologically based, divergent selection causes the evolution of reproductive isolation. There are many empirical examples of this process; however, there exists a poorly characterized stage during which the traits that distinguish species ecologically and reproductively segregate in a single population. By using a combination of genetic mapping, mate-choice experiments, field observations, and population genetics, we studied a butterfly population with a mimetic wing color polymorphism and found that the butterflies exhibited partial, color-based, assortative mate preference. These traits represent the divergent, ecologically based signal and preference components of sexual isolation that usually distinguish incipient and sibling species. The association between behavior and recognition trait in a single population may enhance the probability of speciation and provides an example of the missing link between an interbreeding population and isolated species.

Dispersal and Gene Flow in a Butterfly Species

Populations of the butterfly Euphydryas editha differ in dispersal rates of component individuals. We give evidence that these differences are at least partly genetically based and are the result of long-term selection pressures associated with the detailed ecology of each population. Within this framework, population structure is affected by the distributions of larval and adult resources in space and time, and is described in detail for two populations of contrasting types. We predict genetic consequences of interpopulation differences in dispersal and use our observations of E. editha to illustrate a general discussion of factors affecting dispersal in insects.

Phylogenetic Relationships and Chromosome Number Evolution in Passiflora

Abstract The phylogenetic relationships and chromosomal evolution of the diverse tropical genus Passiflora (Passifloraceae) are explored using data from two chloroplast markers: the rpoC1 intron and the trnL/trnT spacer region. A survey of the presence or absence of the rpoC1 intron in 136 species representing 17 of Killips (1938) 22 subgenera of Passiflora and four other genera in the Passifloraceae revealed intron losses in 46 taxa. A minimum of two losses were confirmed by a parametric bootstrap approach on sequence data from the trnL/trnT chloroplast non-coding region for 61 taxa. The results of phylogenetic analyses of the trnL/trnT sequence data support the reduction of Killips 22 subgenera to four as proposed in a new classification system by Feuillet and MacDougal (2004). The monophyly of the ‘n=6’ and ‘n=9’ chromosomal and morphological groups is strongly supported. In addition, these data indicate that Passiflora biflora, or closely related species, is the likely continental sister to the red-flowered Caribbean taxa, while P. auriculata is weakly supported as the New World sister to the Old World Passifloras. Finally, character optimization of chromosome numbers on the phylogenetic tree supports x=12 as the base chromosome number for Passiflora.

Insect metabolism: Preventing cyanide release from leaves

Organisms that produce hydrogen cyanide gas to protect themselves against predators can do so by the enzymatic breakdown of a class of compounds known as cyanogens (such as cyanogenic glycosides). Here we show how a neotropical butterfly, Heliconius sara, can avoid the harmful effects of the cyanogenic leaves of Passiflora auriculata (passion vine), on which its larvae feed exclusively. To our knowledge this is the first example of an insect that is able to metabolize cyanogens and thereby prevent the release of cyanide. The mechanistic details of this pathway might suggest new ways to make cyanogenic crops more useful as a food source.

Foraging ecology and patterns of diversification in dipteran parasitoids of fire ants in south brazil

1. At least sixteen species of parasitoid flies in the genus Pseudacteon (family Phoridae) attack fire ants in the Solenopsis saevissima subcomplex in South America. Little is known of behavioural or ecological differences among Pseudacteon parasitoids of fire ants, although their coexistence in multispecies communities would suggest that important differences exist. Seven Pseudacteon species in two separate communities were studied in south‐east Brazil. The way in which hosts detect and respond to the presence of parasitoids, attack rates of the parasitoids, and host location behaviour of the parasitoids were examined.

Phorid parasitoids affect foraging activity of Solenopsis richteri under different availability of food in Argentina

1. In Argentina, six species of Pseudacteon parasitoids (Phoridae) attack Solenopsis richteri, one of the two species of South American fire ant that are exotic pests in North America.