Chemosensory communication is essential to insect biology, playing indispensable roles during mate-finding, foraging, and oviposition behaviors. These traits are particularly important during speciation, where chemical perception may serve to establish species barriers. However, identifying genes associated with such complex behavioral traits remains a significant challenge. Through a combination of transcriptomic and genomic approaches, we characterize the genetic architecture of chemoperception and the role of chemosensing during speciation for a young species pair of Heliconius butterflies, Heliconius melpomene and Heliconius cydno . We provide a detailed description of chemosensory gene-expression profiles as they relate to sensory tissue (antennae, legs, and mouthparts), sex (male and female), and life stage (unmated and mated female butterflies). Our results untangle the potential role of chemical communication in establishing barriers during speciation and identify strong candidate genes for mate and host plant choice behaviors. Of the 252 chemosensory genes, HmOBP20 (involved in volatile detection) and HmGr56 (a putative synephrine-related receptor) emerge as strong candidates for divergence in pheromone detection and host plant discrimination, respectively. These two genes are not physically linked to wing-color pattern loci or other genomic regions associated with visual mate preference. Altogether, our results provide evidence for chemosensory divergence between H. melpomene and H. cydno , two rarely hybridizing butterflies with distinct mate and host plant preferences, a finding that supports a polygenic architecture of species boundaries.
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Engaging the Community in Pollinator Research: The Effect of Wing Pattern and Weather on Butterfly Behavior
Abstract Community science, which engages students and the public in data collection and scientific inquiry, is often integrated into conservation and long-term monitoring efforts. However, it has the potential to also introduce the public to, and be useful for, sensory ecology and other fields of study. Here we describe a community science project that exposes participants to animal behavior and sensory ecology using the rich butterfly community of Northwest Arkansas, United States. Butterflies use visual signals to communicate and to attract mates. Brighter colors can produce stronger signals for mate attraction but can also unintentionally attract negative attention from predators. Environmental conditions such as weather can affect visual signaling as well, by influencing the wavelengths of light available and subsequent signal detection. However, we do not know whether the signals butterflies present correlate broadly with how they behave. In this study, we collaborated with hundreds of students and community members at the University of Arkansas (UARK) and the Botanical Gardens of the Ozarks (BGO) for over 3.5 years to examine relationships among wing pattern, weather, time of day, behavior, and flower choice. We found that both weather and wing color influenced general butterfly behavior. Butterflies were seen feeding more on cloudy days than on sunny or partly cloudy days. Brown butterflies fed or sat more often, while white butterflies flew more often relative to other butterfly colors. We also found that there was an interaction between the effects of weather and wing color on butterfly behavior. Furthermore, butterfly color predicted the choice of flower colors that butterflies visited, though this effect was influenced by the observer group (UARK student or BGO participant). These results suggest that flower choice may be associated with butterfly wing pattern, and that different environmental conditions may influence butterfly behavior in wing-pattern–specific ways. They also illustrate one way that public involvement in behavioral studies can facilitate the identification of coarse-scale, community-wide behavioral patterns, and lay the groundwork for future studies of sensory niches.
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- Award ID(s):
- 1937201
- NSF-PAR ID:
- 10310399
- Date Published:
- Journal Name:
- Integrative and Comparative Biology
- Volume:
- 61
- Issue:
- 3
- ISSN:
- 1540-7063
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Unisensory cues are often insufficient for animals to effectively engage in foraging, mating, and predatory activities. In contrast, integration of cues collected from multiple sensory organs enhances the overall perceptual experience and thereby facilitates better decision‐making. Despite the importance of multisensory integration in animals, the field of artificial intelligence (AI) and neuromorphic computing has primarily focused on processing unisensory information. This lack of emphasis on multisensory integration can be attributed to the absence of a miniaturized hardware platform capable of co‐locating multiple sensing modalities and enabling in‐sensor and near‐sensor processing. In this study, this limitation is addressed by utilizing the chemo‐sensing properties of graphene and the photo‐sensing capability of monolayer molybdenum disulfide (MoS2) to create a multisensory platform for visuochemical integration. Additionally, the in‐memory‐compute capability of MoS2memtransistors is leveraged to develop neural circuits that facilitate multisensory decision‐making. The visuochemical integration platform is inspired by intricate courtship of Heliconius butterflies, where female species rely on the integration of visual cues (such as wing color) and chemical cues (such as pheromones) generated by the male butterflies for mate selection. The butterfly‐inspired visuochemical integration platform has significant implications in both robotics and the advancement of neuromorphic computing, going beyond unisensory intelligence and information processing.
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While male mate choice has received sparse attention in comparison to female choice, it occurs often in insects. In addition, male insects may preferentially allocate sperm and ejaculate in response to female quality. Previous research indicates that male Bicyclus anynana butterflies can learn mate preference through prior exposure to females, though naïve males mate randomly. It is unclear whether this preference learning may also influence male sperm and ejaculate allocation after mate selection, or whether males have cryptic mate preference for female wing patterns independent of preference learning. Here we test whether B. anynana males adjust their sperm and ejaculate allocation in response to a learned preference. We also assess whether males exhibit an innate cryptic preference and adjust their sperm and ejaculate in response to female wing pattern. We compared number of eggs laid by females and spermatophore (male butterfly ejaculate) weight in four no-choice treatments: naïve male butterflies (having no prior exposure to females), paired with a 2 or 0-spot female, and experienced male butterflies (having a previous three-hour interaction with a 0-spot female), paired with a 2 or 0-spot female. All females used were naturally 2-spot females, 0-spot females had artificially blocked spots. We found that 0-spot females laid significantly more eggs than 2-spot females, independent of male experience. There was no effect of female phenotype or male experience on spermatophore weight. Our findings suggest that male B. anynana have an innate cryptic preference for 0-spot females, which has been shown in other studies to only be seen as a pre-copulatory preference when enhanced by early experience.more » « less
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null (Ed.)Abstract Background Bird plumage exhibits a diversity of colors that serve functional roles ranging from signaling to camouflage and thermoregulation. However, birds must maintain a balance between evolving colorful signals to attract mates, minimizing conspicuousness to predators, and optimizing adaptation to climate conditions. Examining plumage color macroevolution provides a framework for understanding this dynamic interplay over phylogenetic scales. Plumage evolution due to a single overarching process, such as selection, may generate the same macroevolutionary pattern of color variation across all body regions. In contrast, independent processes may partition plumage and produce region-specific patterns. To test these alternative scenarios, we collected color data from museum specimens of an ornate clade of birds, the Australasian lorikeets, using visible-light and UV-light photography, and comparative methods. We predicted that the diversification of homologous feather regions, i.e., patches, known to be involved in sexual signaling (e.g., face) would be less constrained than patches on the back and wings, where new color states may come at the cost of crypsis. Because environmental adaptation may drive evolution towards or away from color states, we tested whether climate more strongly covaried with plumage regions under greater or weaker macroevolutionary constraint. Results We found that alternative macroevolutionary models and varying rates best describe color evolution, a pattern consistent with our prediction that different plumage regions evolved in response to independent processes. Modeling plumage regions independently, in functional groups, and all together showed that patches with similar macroevolutionary models clustered together into distinct regions (e.g., head, wing, belly), which suggests that plumage does not evolve as a single trait in this group. Wing patches, which were conserved on a macroevolutionary scale, covaried with climate more strongly than plumage regions (e.g., head), which diversified in a burst. Conclusions Overall, our results support the hypothesis that the extraordinary color diversity in the lorikeets was generated by a mosaic of evolutionary processes acting on plumage region subsets. Partitioning of plumage regions in different parts of the body provides a mechanism that allows birds to evolve bright colors for signaling and remain hidden from predators or adapt to local climatic conditions.more » « less
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null (Ed.)Heliconius butterflies have bright patterns on their wings that tell potential predators that they are toxic. As a result, predators learn to avoid eating them. Over time, unrelated species of butterflies have evolved similar patterns to avoid predation through a process known as Müllerian mimicry. Worldwide, there are over 180,000 species of butterflies and moths, most of which have different wing patterns. How do genes create this pattern diversity? And do butterflies use similar genes to create similar wing patterns? One of the genes involved in creating wing patterns is called cortex . This gene has a large region of DNA around it that does not code for proteins, but instead, controls whether cortex is on or off in different parts of the wing. Changes in this non-coding region can act like switches, turning regions of the wing into different colours and creating complex patterns, but it is unclear how these switches have evolved. Butterfly wings get their colour from tiny structures called scales, which each have their own unique set of pigments. In Heliconius butterflies, there are three types of scales: yellow/white scales, black scales, and red/orange/brown scales. Livraghi et al. used a DNA editing technique called CRISPR to find out whether the cortex gene affects scale type. First, Livraghi et al. confirmed that deleting cortex turned black and red scales yellow. Next, they used the same technique to manipulate the non-coding DNA around the cortex gene to see the effect on the wing pattern. This manipulation turned a black-winged butterfly into a butterfly with a yellow wing band, a pattern that occurs naturally in Heliconius butterflies. The next step was to find the mutation responsible for the appearance of yellow wing bands in nature. It turns out that a bit of extra genetic code, derived from so-called ‘jumping genes’, had inserted itself into the non-coding DNA around the cortex gene, ‘flipping’ the switch and leading to the appearance of the yellow scales. Genetic information contains the instructions to generate shape and form in most organisms. These instructions evolve over millions of years, creating everything from bacteria to blue whales. Butterfly wings are visual evidence of evolution, but the way their genes create new patterns isn't specific to butterflies. Understanding wing patterns can help researchers to learn how genetic switches control diversity across other species too.more » « less
- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/icb/icab153
