Weighting of sensory cues reflect changing patterns of visual investment during ecological divergence in butterflies.

Integrating information across sensory modalities enables animals to orchestrate a wide range of complex behaviours. The relative importance placed on one sensory modality over another reflects the reliability of cues in a particular environment and corresponding differences in neural investment. As populations diverge across environmental gradients, the reliability of sensory cues may shift, favouring divergence in neural investment and the weight given to different sensory modalities.

Selection drives divergence of eye morphology in sympatric Heliconius butterflies.

When populations experience different sensory conditions, natural selection may favor sensory system divergence, affecting peripheral structures and/or downstream neural pathways. We characterized the outer eye morphology of sympatric Heliconius butterflies from different forest types and their first-generation reciprocal hybrids to test for adaptive visual system divergence and hybrid disruption. In Panama, Heliconius cydno occurs in closed forests, whereas Heliconius melpomene resides at the forest edge.

Adaptive introgression of a visual preference gene.

Visual preferences are important drivers of mate choice and sexual selection, but little is known of how they evolve at the genetic level. In this study, we took advantage of the diversity of bright warning patterns displayed by butterflies, which are also used during mate choice. Combining behavioral, population genomic, and expression analyses, we show that two species have evolved the same preferences for red patterns by exchanging genetic material through hybridization.

Divergent warning patterns influence male and female mating behaviours in a tropical butterfly.

Traits under divergent ecological selection that also function during mating can be important in maintaining species boundaries. Few studies have considered mutual mate choice, where both males and females base mating decisions on the same trait. Wing colouration in Heliconius butterflies evolved as a warning signal but also functions as a mating cue.

Parallel shifts in flight-height associated with altitude across incipient Heliconius species.

Vertical gradients in microclimate, resource availability, and interspecific interactions are thought to underly stratification patterns in tropical insect communities. However, only a few studies have explored the adaptive significance of vertical space use during the early stages of reproductive isolation. We analysed flight-height variation across speciation events in Heliconius butterflies, representing parallel colonizations of high-altitude forest.

Quantifying visual acuity in butterflies.

butterflies are well-known for their colourful wing patterns, which advertise distastefulness to potential predators and are used during mate choice. However, the relative importance of different aspects of these signals will depend on the visual abilities of and their predators. Previous studies have investigated colour sensitivity and neural anatomy, but visual acuity (the ability to perceive detail) has not been studied in these butterflies.

The Sensory Ecology of Speciation.

In this work, we explore the potential influence of sensory ecology on speciation, including but not limited to the concept of sensory drive, which concerns the coevolution of signals and sensory systems with the local environment. The sensory environment can influence individual fitness in a variety of ways, thereby affecting the evolution of both pre- and postmating reproductive isolation. Previous work focused on sensory drive has undoubtedly advanced the field, but we argue that it may have also narrowed our understanding of the broader influence of the sensory ecology on speciation.

Genetics and the Evolution of Prezygotic Isolation.

The significance of prezygotic isolation for speciation has been recognized at least since the Modern Synthesis. However, fundamental questions remain. For example, how are genetic associations between traits that contribute to prezygotic isolation maintained? What is the source of genetic variation underlying the evolution of these traits? And how do prezygotic barriers affect patterns of gene flow? We address these questions by reviewing genetic features shared across plants and animals that influence prezygotic isolation.

Oviposition behavior is not affected by ultraviolet light in a butterfly with sexually-dimorphic expression of a UV-sensitive opsin.

Animal vision is important for mediating multiple complex behaviors. In butterflies, vision guides fundamental behaviors such as oviposition, foraging, and mate choice. Color vision in involves ultraviolet (UV), blue and long-wavelength-sensitive photoreceptors (opsins).

Parallel evolution of behavior, physiology, and life history associated with altitudinal shifts in forest type in Heliconius butterflies.

Parallel evolution of morphological traits is widely reported, providing evidence for the role of local conditions in driving adaptive divergence. Comparatively, fewer studies have tested for parallelism in behavior, and it is less clear to what extent heritable behavioral shifts contribute to adaptive divergence. We exploit repeated incipient speciation across altitudinal gradients to explore behavior and physiology in Heliconius butterflies adapted to high-elevation.

Does sexual conflict contribute to the evolution of novel warning patterns?

Why warning patterns are so diverse is an enduring evolutionary puzzle. Because predators associate particular patterns with unpleasant experiences, an individual's predation risk should decrease as the local density of its warning pattern increases, promoting pattern monomorphism. Distasteful Heliconius butterflies are known for their diversity of warning patterns.

Evolution of physical linkage between loci controlling ecological traits and mating preferences.

Coupling of multiple barriers to gene-flow, such as divergent local adaptation and reproductive isolation, facilitates speciation. However, alleles at loci that contribute to barrier effects can be dissociated by recombination. Models of linkage between diverging alleles often consider elements that reduce recombination, such as chromosomal inversions and alleles that modify recombination rate between existing loci.

Homage to Felsenstein 1981, or why are there so few/many species?

If there are no constraints on the process of speciation, then the number of species might be expected to match the number of available niches and this number might be indefinitely large. One possible constraint is the opportunity for allopatric divergence. In 1981, Felsenstein used a simple and elegant model to ask if there might also be genetic constraints.

Light environment influences mating behaviours during the early stages of divergence in tropical butterflies.

Speciation is facilitated when traits under divergent selection also act as mating cues. Fluctuations in sensory conditions can alter signal perception independently of adaptation to the broader sensory environment, but how this fine-scale variation may constrain or promote behavioural isolation has received little attention. The warning patterns of butterflies are under selection for aposematism and act as mating cues.

Neural divergence and hybrid disruption between ecologically isolated butterflies.

The importance of behavioral evolution during speciation is well established, but we know little about how this is manifest in sensory and neural systems. A handful of studies have linked specific neural changes to divergence in host or mate preferences associated with speciation. However, the degree to which brains are adapted to local environmental conditions, and whether this contributes to reproductive isolation between close relatives that have diverged in ecology, remains unknown.

A novel terpene synthase controls differences in anti-aphrodisiac pheromone production between closely related Heliconius butterflies.

Plants and insects often use the same compounds for chemical communication, but not much is known about the genetics of convergent evolution of chemical signals. The terpene (E)-β-ocimene is a common component of floral scent and is also used by the butterfly Heliconius melpomene as an anti-aphrodisiac pheromone. While the biosynthesis of terpenes has been described in plants and microorganisms, few terpene synthases (TPSs) have been identified in insects.

Clustering of loci controlling species differences in male chemical bouquets of sympatric butterflies.

The degree to which loci promoting reproductive isolation cluster in the genome-that is, the genetic architecture of reproductive isolation-can influence the tempo and mode of speciation. Tight linkage between these loci can facilitate speciation in the face of gene flow. Pheromones play a role in reproductive isolation in many Lepidoptera species, and the role of endogenously produced compounds as secondary metabolites decreases the likelihood of pleiotropy associated with many barrier loci.

Visual mate preference evolution during butterfly speciation is linked to neural processing genes.

Many animal species remain separate not because their individuals fail to produce viable hybrids but because they "choose" not to mate. However, we still know very little of the genetic mechanisms underlying changes in these mate preference behaviours. Heliconius butterflies display bright warning patterns, which they also use to recognize conspecifics.

Species specificity and intraspecific variation in the chemical profiles of butterflies across a large geographic range.

In many animals, mate choice is important for the maintenance of reproductive isolation between species. Traits important for mate choice and behavioral isolation are predicted to be under strong stabilizing selection within species; however, such traits can also exhibit variation at the population level driven by neutral and adaptive evolutionary processes. Here, we describe patterns of divergence among androconial and genital chemical profiles at inter- and intraspecific levels in mimetic butterflies.

Hybridization and transgressive exploration of colour pattern and wing morphology in Heliconius butterflies.

Hybridization can generate novel phenotypes distinct from those of parental lineages, a phenomenon known as transgressive trait variation. Transgressive phenotypes might negatively or positively affect hybrid fitness, and increase available variation. Closely related species of Heliconius butterflies regularly produce hybrids in nature, and hybridization is thought to play a role in the diversification of novel wing colour patterns despite strong stabilizing selection due to interspecific mimicry.

A major locus controls a biologically active pheromone component in Heliconius melpomene.

Understanding the production, response, and genetics of signals used in mate choice can inform our understanding of the evolution of both intraspecific mate choice and reproductive isolation. Sex pheromones are important for courtship and mate choice in many insects, but we know relatively little of their role in butterflies. The butterfly Heliconius melpomene uses a complex blend of wing androconial compounds during courtship.

Male pheromone composition depends on larval but not adult diet in .

1. Condition-dependent traits can act as honest signals of mate quality, with fitter individuals being able to display preferred phenotypes. Nutrition is known to be an important determinant of individual condition, with diet known to affect many secondary sexual traits.

Genetic dissection of assortative mating behavior.

The evolution of new species is made easier when traits under divergent ecological selection are also mating cues. Such ecological mating cues are now considered more common than previously thought, but we still know little about the genetic changes underlying their evolution or more generally about the genetic basis for assortative mating behaviors. Both tight physical linkage and the existence of large-effect preference loci will strengthen genetic associations between behavioral and ecological barriers, promoting the evolution of assortative mating.

Male sex pheromone components in butterflies released by the androconia affect female choice.

Sex-specific pheromones are known to play an important role in butterfly courtship, and may influence both individual reproductive success and reproductive isolation between species. Extensive ecological, behavioural and genetic studies of butterflies have made a substantial contribution to our understanding of speciation. Male pheromones, although long suspected to play an important role, have received relatively little attention in this genus.