Richard M. Merrill

Sexually selected traits predict patterns of species richness in a diverse clade of suboscine birds.

Whether sexual selection acts as an “engine of speciation” is controversial. Some studies suggest that it promotes the evolution of reproductive isolation, while others find no relationship between sexual selection and species richness. However, the explanatory power of previous models may have been constrained because they employed coarse‐scale, between‐family comparisons and used mating systems and morphological cues as surrogates for sexual selection. In birds, an obvious missing predictor is song, a sexually selected trait that functions in mate choice and reproductive isolation. We investigated the extent to which plumage dichromatism and song structure predicted species richness in a diverse family of Neotropical suboscine birds, the antbirds (Thamnophilidae). These analyses revealed a positive relationship between the intensity of sexual selection and diversity: genera with higher levels of dichromatism and lower‐pitched, more complex songs contained greater numbers of species. This relationship held when controlling for phylogeny and was strengthened by the inclusion of subspecies, suggesting that sexual selection has played a role in the diversification of antbirds. This is the first study to reveal correlations between song structure and species diversity, emphasizing the importance of acoustic signals, and within‐family analyses, in comparative studies of sexual selection.

Disruptive ecological selection on a mating cue

Adaptation to divergent ecological niches can result in speciation. Traits subject to disruptive selection that also contribute to non-random mating will facilitate speciation with gene flow. Such ‘magic’ or ‘multiple-effect’ traits may be widespread and important for generating biodiversity, but strong empirical evidence is still lacking. Although there is evidence that putative ecological traits are indeed involved in assortative mating, evidence that these same traits are under divergent selection is considerably weaker. Heliconius butterfly wing patterns are subject to positive frequency-dependent selection by predators, owing to aposematism and Müllerian mimicry, and divergent colour patterns are used by closely related species to recognize potential mates. The amenability of colour patterns to experimental manipulation, independent of other traits, presents an excellent opportunity to test their role during speciation. We conducted field experiments with artificial butterflies, designed to match natural butterflies with respect to avian vision. These were complemented with enclosure trials with live birds and real butterflies. Our experiments showed that hybrid colour-pattern phenotypes are attacked more frequently than parental forms. For the first time, we demonstrate disruptive ecological selection on a trait that also acts as a mating cue.

MATE PREFERENCE ACROSS THE SPECIATION CONTINUUM IN A CLADE OF MIMETIC BUTTERFLIES

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.

Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies.

Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene, also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which ‘speciation genes’ are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.

The diversification of Heliconius butterflies: what have we learned in 150 years?

Research into Heliconius butterflies has made a significant contribution to evolutionary biology. Here, we review our understanding of the diversification of these butterflies, covering recent advances and a vast foundation of earlier work. Whereas no single group of organisms can be sufficient for understanding lifes diversity, after years of intensive study, research into Heliconius has addressed a wide variety of evolutionary questions. We first discuss evidence for widespread gene flow between Heliconius species and what this reveals about the nature of species. We then address the evolution and diversity of warning patterns, both as the target of selection and with respect to their underlying genetic basis. The identification of major genes involved in mimetic shifts, and homology at these loci between distantly related taxa, has revealed a surprising predictability in the genetic basis of evolution. In the final sections, we consider the evolution of warning patterns, and Heliconius diversity more generally, within a broader context of ecological and sexual selection. We consider how different traits and modes of selection can interact and influence the evolution of reproductive isolation.

The gene cortex controls mimicry and crypsis in butterflies and moths

The wing patterns of butterflies and moths (Lepidoptera) are diverse and striking examples of evolutionary diversification by natural selection1,2. Lepidopteran wing colour patterns are a key innovation, consisting of arrays of coloured scales. We still lack a general understanding of how these patterns are controlled and if there is any commonality across the 160,000 moth and 17,000 butterfly species. Here, we identify a gene, cortex, through fine-scale mapping using population genomics and gene expression analyses, which regulates pattern switches in multiple species across the mimetic radiation in Heliconius butterflies. cortex belongs to a fast evolving subfamily of the otherwise highly conserved fizzy family of cell cycle regulators3, suggesting that it most likely regulates pigmentation patterning through regulation of scale cell development. In parallel with findings in the peppered moth (Biston betularia)4, our results suggest that this mechanism is common within Lepidoptera and that cortex has become a major target for natural selection acting on colour and pattern variation in this group of insects.

The biology of color

In living color Animals live in a colorful world, but we rarely stop to think about how this color is produced and perceived, or how it evolved. Cuthill et al. review how color is used for social signals between individual animals and how it affects interactions with parasites, predators, and the physical environment. New approaches are elucidating aspects of animal coloration, from the requirements for complex cognition and perception mechanisms to the evolutionary dynamics surrounding its development and diversification. Science, this issue p. eaan0221 BACKGROUND The interdisciplinary field of animal coloration is growing rapidly, spanning questions about the diverse ways that animals use pigments and structures to generate color, the underlying genetics and epigenetics, the perception of color, how color information is integrated with information from other senses, and general principles underlying color’s evolution and function. People working in the field appreciate linkages between these parallel lines of enquiry, but outsiders need the easily navigable roadmap that we provide here. ADVANCES In the past 20 years, the field of animal coloration research has been propelled forward by technological advances that include spectrophotometry, digital imaging, computational neuroscience, innovative laboratory and field studies, and large-scale comparative analyses, which are allowing new questions to be asked. For example, we can now pose questions about the evolution of camouflage based on what a prey’s main predator can see, and we can start to appreciate that gene changes underlying color production have occurred in parallel in unrelated species. Knowledge of the production, perception, and evolutionary function of coloration is poised to make contributions to areas as diverse as medicine, security, clothing, and the military, but we need to take stock before moving forward. OUTLOOK Here, a group of evolutionary biologists, behavioral ecologists, psychologists, optical physicists, visual physiologists, geneticists, and anthropologists review this diverse area of science, daunting to the outsider, and set out what we believe are the key questions for the future. These are how nanoscale structures are used to manipulate light; how dynamic changes in coloration occur on different time scales; the genetics of coloration (including key innovations and the extent of parallel changes in different lineages); alternative perceptions of color by different species (including wavelengths that we cannot see, such as ultraviolet); how color, pattern, and motion interact; and how color works together with other modalities, especially odor. From an adaptive standpoint, color can serve several functions, and the resulting patterns frequently represent a trade-off among different evolutionary drivers, some of which are nonvisual (e.g., photoprotection). These trade-offs can vary between individuals within the same population, and color can be altered strategically on different time scales to serve different purposes. Lastly, interspecific differences in coloration, sometimes even observable in the fossil record, give insights into trait evolution. The biology of color is a field that typifies modern research: curiosity-led, technology-driven, multilevel, interdisciplinary, and integrative. Spectacular changes to color and morphology in a cuttlefish. Color can conceal or reveal. The giant Australian cuttlefish (Sepia apama) alters the relative size of its pigment-bearing chromatophores and warps its muscular skin to switch between camouflage mode (top) and communication mode (bottom) in under a second. Photos:

Divergent warning patterns contribute to assortative mating between incipient Heliconius species

Theoretical models suggest that traits under divergent ecological selection, which also contribute to assortative mating, will facilitate speciation with gene flow. Evidence for these so-called “magic traits” now exists across a range of taxa. However, their importance during speciation will depend on the extent to which they contribute to reproductive isolation. Addressing this requires experiments to determine the exact cues involved as well as estimates of assortative mating in the wild. Heliconius butterflies are well known for their diversity of bright warning color patterns, and their amenability to experimental manipulation has provided an excellent opportunity to test their role in reproductive isolation. Here, we reveal that divergent color patterns contribute to mate recognition between the incipient species Heliconius himera and H. erato, a taxon pair for which assortative mating by color pattern has been demonstrated among wild individuals: First, we demonstrate that males are more likely to attempt to mate conspecific females; second, we show that males are more likely to approach pinned females that share their own warning pattern. These data are valuable as these taxa likely represent the early stages of speciation, but unusually also allow comparisons with rates of interbreeding between divergent ecologically relevant phenotypes measured in the wild.

Brain composition in Heliconius butterflies, posteclosion growth and experience‐dependent neuropil plasticity

Behavioral and sensory adaptations are often reflected in the differential expansion of brain components. These volumetric differences represent changes in cell number, size, and/or connectivity, which may denote changes in the functional and evolutionary relationships between different brain regions, and between brain composition and behavioral ecology. Here we describe the brain composition of two species of Heliconius butterflies, a long‐standing study system for investigating ecological adaptation and speciation. We confirm a previous report of a striking volumetric expansion of the mushroom body, and explore patterns of differential posteclosion and experience‐dependent plasticity between different brain regions. This analysis uncovers age‐ and experience‐dependent posteclosion mushroom body growth comparable to that in foraging Hymenoptera, but also identifies plasticity in several other neuropils. An interspecific analysis indicates that Heliconius display a remarkably large investment in mushroom bodies for a lepidopteran, and indeed rank highly compared to other insects. Our analyses lay the foundation for future comparative and experimental analyses that will establish Heliconius as a valuable case study in evolutionary neurobiology. J. Comp. Neurol. 524:1747–1769, 2016.

Müllerian Mimicry: Sharing the Load Reduces the Legwork

Color pattern mimicry has long been held up as a powerful example of natural selection. A recent study supports the theory by describing Müllerian mimicry rings in Appalachian millipedes that are analogous to those observed in tropical butterflies.