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Cycads are an ancient group of tropical gymnosperms that are toxic to most animals - including humans - though the larvae of many moths and butterflies (order: Lepidoptera) feed on cycads with apparent immunity. These insects belong to distinct lineages with varying degrees of specialisation and diverse feeding ecologies, presenting numerous opportunities for comparative studies of chemically mediated eco-evolutionary dynamics. This review presents the first evolutionary evaluation of cycad-feeding among Lepidoptera along with a comprehensive review of their ecology. Our analysis suggests that multiple lineages have independently colonised cycads from angiosperm hosts, yet only a few clades appear to have radiated following their transitions to cycads. Defensive traits are likely important for diversification, as many cycad specialists are warningly coloured and sequester cycad toxins. The butterfly family Lycaenidae appears to be particularly predisposed to cycad-feeding and several cycadivorous lycaenids are warningly coloured and chemically defended. Cycad-herbivore interactions provide a promising but underutilised study system for investigating plant-insect coevolution, convergent and divergent adaptations, and the multi-trophic significance of defensive traits; therefore the review ends by suggesting specific research gaps that would be fruitfully addressed in Lepidoptera and other cycad-feeding insects.

[Formula: see text]-methylamino-L-alanine (BMAA) is a neurotoxic non-protein amino acid found in the tissues of cycad plants. The demonstrated toxicity of BMAA to diverse organisms, including humans, is widely assumed to imply a defensive function of BMAA against herbivores; however, this hypothesis has not previously been tested in an ecologically relevant system. We investigated the effects of dietary BMAA, across a range of dosages matching and exceeding levels typically present in cycad leaves, on the feeding preferences and performance of a generalist lepidopteran herbivore (Spodoptera littoralis).We observed no effects of dietary BMAA on the survival or development of S. littoralis larvae, nor any larval preference between BMAA-laced and control diets. These findings suggest that BMAA in cycad tissues does not deter feeding by insect herbivores, raising questions about other potential physiological or ecological functions of this compound.

Male butterflies in the hyperdiverse tribe Eumaeini possess an unusually complex and diverse repertoire of secondary sexual characteristics involved in pheromone production and dissemination. Maintaining multiple sexually selected traits is likely to be metabolically costly, potentially resulting in trade-offs in the evolution of male signals. However, a phylogenetic framework to test hypotheses regarding the evolution and maintenance of male sexual traits in Eumaeini has been lacking. Here, we infer a comprehensive, time-calibrated phylogeny from 379 loci for 187 species representing 91% of the 87 described genera. Eumaeini is a monophyletic group that originated in the late Oligocene and underwent rapid radiation in the Neotropics. We examined specimens of 818 of the 1096 described species (75%) and found that secondary sexual traits are present in males of 91% of the surveyed species. Scent pads and scent patches on the wings and brush organs associated with the genitalia were probably present in the common ancestor of Eumaeini and are widespread throughout the tribe. Brush organs and scent pads are negatively correlated across the phylogeny, exhibiting a trade-off in which lineages with brush organs are unlikely to regain scent pads and vice versa. In contrast, scent patches seem to facilitate the evolution of scent pads, although they are readily lost once scent pads have evolved. Our results illustrate the complex interplay between natural and sexual selection in the origin and maintenance of multiple male secondary sexual characteristics and highlight the potential role of sexual selection spurring diversification in this lineage., Proceedings of the Royal Society B: Biological Sciences, 288 (1950), ISSN:0080-4649, ISSN:0950-1193, ISSN:1471-2954, ISSN:0962-8452

Color vision has evolved multiple times in both vertebrates and invertebrates and is largely determined by the number and variation in spectral sensitivities of distinct opsin subclasses. However, because of the difficulty of expressing long-wavelength (LW) invertebrate opsins in vitro, our understanding of the molecular basis of functional shifts in opsin spectral sensitivities has been biased toward research primarily in vertebrates. This has restricted our ability to address whether invertebrate G(q) protein-coupled opsins function in a novel or convergent way compared to vertebrate G(t) opsins. Here we develop a robust heterologous expression system to purify invertebrate rhodopsins, identify specific amino acid changes responsible for adaptive spectral tuning, and pinpoint how molecular variation in invertebrate opsins underlie wavelength sensitivity shifts that enhance visual perception. By combining functional and optophysiological approaches, we disentangle the relative contributions of lateral filtering pigments from red-shifted LW and blue short-wavelength opsins expressed in distinct photoreceptor cells of individual ommatidia. We use in situ hybridization to visualize six ommatidial classes in the compound eye of a lycaenid butterfly with a four-opsin visual system. We show experimentally that certain key tuning residues underlying green spectral shifts in blue opsin paralogs have evolved repeatedly among short-wavelength opsin lineages. Taken together, our results demonstrate the interplay between regulatory and adaptive evolution at multiple G(q) opsin loci, as well as how coordinated spectral shifts in LW and blue opsins can act together to enhance insect spectral sensitivity at blue and red wavelengths for visual performance adaptation.

Though once considered extinct in Florida, the Eumaeus atala butterfly (Poey) (Lepidoptera: Lycaenidae) has made a slow but steady recovery thanks to grassroots conservation efforts targeting the butterfly and its only native foodplant, the cycad Zamia integrifolia L.f. (Cycadales: Zamiaceae). A robust E. atala population occurs at the Montgomery Botanical Center, a research and conservation facility in Coral Gables, Florida, USA, that cultivates a living collection of global cycads, many of which are critically endangered in the wild. Since the early 2000s, the E. atala population at the Montgomery Botanical Center has grown and adopted an expanded host range, much to the detriment of the plants; both native and exotic cycads incur consistent and severe damage from larval herbivory. This presents a complex situation in which in situ butterfly conservation conflicts with ex situ cycad conservation. Here we describe the local population of E. atala at the Montgomery Botanical Center, suggest testable hypotheses for explaining the butterfly’s localized abundance, and discuss implications for butterfly and cycad conservation efforts in Florida. Sumario Aunque se le considero localmente extinta en la Florida, la mariposa Eumaeus atala (Poey) (Lepidoptera: Lycaenidae) ha tenido una recuperacion lenta pero constante gracias a los esfuerzos de conservacion dirigidos a la mariposa y su unica planta alimenticia nativa, la cicada Zamia integrifolia L.f. (Cycadales: Zamiaceae). Una poblacion robusta de E. atala se encuentra en el Centro Botanico de Montgomery, una instalacion de investigacion y conservacion en Coral Gables, Florida, EE.UU., que cultiva una coleccion viviente de cicadas globales, muchas de las cuales estan en peligro critico en la naturaleza. Desde el principio de la decada del 2000, la poblacion de E. atala en el Centro Botanico de Montgomery ha crecido y ha adoptado un rango de hospederos mas amplio, en detrimento de las plantas; tanto las cicadas nativas como las exoticas sufren un dano constante y severo por la herbivoria de las larvas. Esto presenta una situacion compleja en la que la conservacion de mariposas in situ entra en conflicto con la conservacion ex situ de las cicadas. Aqui describimos la poblacion local de E. atala en el Centro Botanico de Montgomery, sugerimos hipotesis comprobables para explicar la abundancia localizada de mariposas y discutimos las implicaciones para los esfuerzos de conservacion de mariposas y cicadas en Florida. Key Words: Eumaeus atala; Zamia integrifolia; coontie; conservation; pest management View this article in BioOne

Colour vision is largely mediated by changes in number, expression, and spectral properties of rhodopsins, but the genetic mechanisms underlying adaptive shifts in spectral sensitivity remain largely unexplored. Usingin vivophotochemistry, optophysiology, andin vitrofunctional assays, we link variation in eye spectral sensitivity at long wavelengths to species-specific absorbance spectra for LW opsins in lycaenid butterflies. In addition to loci specifying an ancestral green-absorbing rhodopsin with maximum spectral sensitivity (λmax) at 520-530 nm inCallophrys sheridaniiandCelastrina ladon, we find a novel form of red-shifted LW rhodopsin at λmax= 565-570 nm inArhopala japonicaandEumaeus atala. Furthermore, we show thatCa. sheridaniiandCe. ladonexhibit a smaller bathochromic shift at BRh2 (480-489 nm), and with the ancestral LW rhodopsin, cannot perceive visible red light beyond 600 nm. In contrast, molecular variation at the LW opsin inA. japonicaandE. atalais coordinated with tuning of the blue opsin that also shifts sensitivity to longer wavelengths enabling colour discrimination up to 617 nm. We then useE. atalaas a model to examine the interplay between red and blue spectral sensitivity. Owing to blue duplicate expression, the spatial distribution of opsin mRNAs within an ommatidium defines an expanded retinal stochastic mosaic of at least six opsin-based photoreceptor classes. Our mutagenesisin vitroassays with BRh1 (λmax= 435 nm) chimeric blue rhodopsins reveal four main residues contributing to the 65 nm bathochromic shift towards BRh2 (λmax= 500 nm). Adaptations in this four-opsin visual system are relevant for discrimination of conspecific reflectance spectra inE. atala. Together, these findings illustrate how functional changes at multiple rhodopsins contribute to the evolution of a broader spectral sensitivity and adaptation in visual performance.Significance StatementRhodopsins are photosensitive protein molecules that absorb specific wavelengths of incoming light and convey colour information in the visual system. We show that molecular evolution in a green insect opsin gene resulted in a shift in its maximal absorbance peak, enabling some lycaenid butterflies to use spectral energy of longer wavelengths (LW) to discriminate colours in the red spectrum better than relatives bearing ancestral green LW rhodopsins. Lycaenids also evolved a duplicate blue opsin gene, and we illustrate an example where species equipped with red LW rhodopsins shifted their blue sensitivity peak to longer wavelengths due to changes in several blue-tuning residues that have evolved repeatedly in different insect lineages. We demonstrate how changes at multiple vision genes in the insect eye effectively create a coordinated mechanism expanding spectral sensitivity for visually guided behaviours such as selecting host plants and mates.

International audience; Evading predators is a fundamental aspect of the ecology and evolution of all prey animals. In studying the influence of prey traits on predation risk, previous researchers have shown that crypsis reduces attack rates on resting prey, predation risk increases with increased prey activity, and rapid locomotion reduces attack rates and increases chances of surviving predator attacks. However, evidence for these conclusions is nearly always based on observations of selected species under artificial conditions. In nature, it remains unclear how defensive traits such as crypsis, activity levels, and speed influence realized predation risk across species in a community. Whereas direct observations of predator-prey interactions in nature are rare, insight can be gained by quantifying bodily damage caused by failed predator attacks. 2). We quantified how butterfly species traits affect predation risk in nature by determining how defensive traits correlate with wing damage caused by failed predation attempts, thereby providing the first robust multi-species comparative analysis of predator-induced bodily damage in wild animals. 3). For 34 species of fruit-feeding butterflies in an African forest, we recorded wing damage and quantified crypsis, activity levels, and flight speed. We then tested for correlations between damage parameters and species traits using comparative methods that account for measurement error. 4). We detected considerable differences in the extent, location, and symmetry of wing surface loss among species, with smaller differences between sexes. We found that males (but not females) of species that flew faster had substantially less wing surface loss. However, we found no correlation between cryptic colouration and symmetrical wing surface loss across species. In species in which males appeared to be more active than females, males had a lower proportion of symmetrical wing surface loss than females. 5). Our results provide evidence that activity greatly influences the probability of attacks and that flying rapidly is effective for escaping pursuing predators in the wild, but we did not find evidence that cryptic species are less likely to be attacked while at rest.

Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein‐rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars’ surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development., Ecology and Evolution, 9 (8), ISSN:2045-7758

Both above- and below-ground interspecific interactions contribute to ecosystem functioning in terrestrial systems, and the integration of below- and above-ground interactions is crucial for deepening our knowledge of nutrient cycling and community dynamics in terrestrial ecosystems. The present study explored the effects of plant–microbe interactions on aphid honeydew quality and quantity and important factors mediating ant–aphid mutualisms and below-ground nutrient dynamics. Soybean aphids (Aphis glycines) were inoculated onto two closely related strains of soybean plants: a nodulating strain that associates with rhizobia and a non-nodulating strain that does not harbor any nitrogen-fixing bacteria. As expected, prior to aphid inoculation, nodulating plants were significantly taller and had more leaves than non-nodulating plants. Aphids feeding on nodulating strains were found to reach slightly larger colony sizes and produce honeydew with significantly different sugar profiles than those feeding on non-nodulating plants. The honeydew collected from aphid colonies feeding on nodulating plants contained 160 % more total sugars than honeydew collected from colonies feeding on non-nodulating plants, but there was no difference in total amino acid-N content in honeydew from colonies feeding on the different plant strains. We discuss the implications of honeydew composition for nutrient cycling and community dynamics and suggest areas of future research to elucidate the consequences of altered aphid honeydew composition on ecosystem properties.

Herbivores possess many counteradaptations to plant defenses, and a growing body of research describes the role of symbiotic gut bacteria in mediating herbivorous diets among insects. However, persistent bacterial symbioses have not been found in Lepidoptera, despite the fact that perhaps 99% of the species in this order are herbivorous. We surveyed bacterial communities in the guts of larvae from 31 species of lycaenid butterflies whose caterpillars had diets ranging from obligate carnivory to strict herbivory. Contrary to our expectations, we found that the bacterial communities of carnivorous and herbivorous caterpillars do not differ in richness, diversity, or composition. Many of the observed bacterial genera are commonly found in soil and plant surfaces, and we detected known homopteran endosymbionts in the guts of homopterophagous species, suggesting that larvae acquire gut bacteria from their food and environment. These results indicate that lycaenid butterflies do not rely on specific bacterial symbioses to mediate their diverse diets, and provide further evidence of taxonomically depauperate bacterial communities among Lepidoptera.