The leaf-footed cactus bug is not a cactus specialist: Narnia femorata feeds, fights, and mates on thistle.

Novel host plants are incorporated into the diets of phytophagous insects when females oviposit and juveniles feed and survive on them. A change in diet, however, can have morphological consequences. We recently found a population of the leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae), a historical cactus specialist, living and feeding on Cirsium thistle. We also found adults breeding and males using their enlarged hind legs (i.e., weapons) in male-male combat on thistle. When we compared this thistle population with a population feeding on cactus, we found that both populations had similar body and weapon sizes as well as weapon composition. However, the population living on thistle had longer mouthparts than the population found on cactus, although this difference only occurred at larger body sizes. This difference in adult mouthpart size is likely a result of the juvenile rearing environment (i.e., thistle or cactus). However, genetic differences may also affect this trait. Our results provide some interesting avenues for future research (e.g., a reciprocal transplant experiment) in a species with a recent host range expansion.

Inbreeding depression in a sexually selected weapon and the homologue in females.

Theory predicts that traits with heightened condition dependence, such as sexually selected traits, should be affected by inbreeding to a greater degree than other traits. The presence of environmental stress may compound the negative consequences of inbreeding depression. In this study, we examined inbreeding depression across multiple traits and whether it increased with a known form of environmental stress. We conducted our experiment using both sexes of the sexually dimorphic leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae). Adult male cactus bugs have enlarged hind legs used as weapons in male-male contests; these traits, and their homologue in females, have been previously found to exhibit high condition dependence. In this study, we employed a small developmental group size as an environmental stress challenge. Nymph N. femorata aggregate throughout their juvenile stages, and previous work has shown the negative effects of small group size on survivorship and body size. We found evidence of inbreeding depression for survival and seven of the eight morphological traits measured in both sexes. Inbreeding depression was higher for the size of the male weapon and the female homolog. Additionally, small developmental group size negatively affected survival to adulthood. However, small group size did not magnify the effects of inbreeding on morphological traits. These findings support the hypothesis that traits with heightened condition dependence exhibit higher levels of inbreeding depression.

The evolution of multi-component weapons in the superfamily of leaf-footed bugs.

Sexually selected weapons, such as the antlers of deer, claws of crabs, and tusks of beaked whales, are strikingly diverse across taxa and even within groups of closely related species. Phylogenetic comparative studies have typically taken a simplified approach to investigate the evolution of weapon diversity, examining the gains and losses of entire weapons, major shifts in size or type, or changes in location. Less understood is how individual weapon components evolve and assemble into a complete weapon. We addressed this question by examining weapon evolution in the diverse, multi-component hind-leg and body weapons of leaf-footed bugs, superfamily Coreoidea (Hemiptera: Heteroptera). Male leaf-footed bugs use their morphological weapons to fight for access to mating territories. We used a large multilocus dataset comprised of ultraconserved element loci for 248 species and inferred evolutionary transitions among component states using ancestral state estimation. Our results suggest that weapons added components over time with some evidence of a cyclical evolutionary pattern-gains of components followed by losses and then gains again. Furthermore, our best estimate indicated that certain trait combinations evolved repeatedly across the phylogeny, suggesting that they function together in battle or that they are genetically correlated. This work reveals the remarkable and dynamic evolution of weapon form in the leaf-footed bugs and provides insights into weapon assembly and disassembly over evolutionary time.

Adult presence does not ameliorate juvenile feeding challenges in a leaf-footed bug.

Herbivores often grapple with structural defences in their host plants, which may pose especially difficult challenges for juveniles due to their underdeveloped feeding morphology. The degree to which juvenile herbivore survival is limited by structural defences as well as the strategies used to overcome them are not well understood. We hypothesized that juveniles benefit from feeding near adults because adults pierce through physical barriers while feeding, enabling juveniles to access nutrients that they otherwise could not. We tested this feeding facilitation hypothesis in the leaf-footed bug Leptoglossus zonatus (Hemiptera: Coreidae). Bugs were raised with an adult or a juvenile conspecific and fed a diet of pecans with or without shells. As predicted, we found that juveniles suffered greater mortality when fed nuts with shells than when fed nuts without shells. Contrary to our expectations, the presence of an adult feeding on the same nut did not lessen this effect. Therefore, the presence of an adult does not ameliorate the feeding difficulties faced by juvenile L. zonatus, despite evidence for feeding facilitation in related insect species. This study adds to our understanding of how host plant defences can limit the survival of even highly generalist herbivores.

Evolution of stridulatory mechanisms: vibroacoustic communication may be common in leaf-footed bugs and allies (Heteroptera: Coreoidea).

Intra- and interspecific communication is crucial to fitness via its role in facilitating mating, territoriality and defence. Yet, the evolution of animal communication systems is puzzling-how do they originate and change over time? Studying stridulatory morphology provides a tractable opportunity to deduce the origin and diversification of a communication mechanism. Stridulation occurs when two sclerotized structures rub together to produce vibratory and acoustic (vibroacoustic) signals, such as a cricket 'chirp'. We investigated the evolution of stridulatory mechanisms in the superfamily Coreoidea (Hemiptera: Heteroptera), a group of insects known for elaborate male fighting behaviours and enlarged hindlegs. We surveyed a large sampling of taxa and used a phylogenomic dataset to investigate the evolution of stridulatory mechanisms. We identified four mechanisms, with at least five evolutionary gains. One mechanism, occurring only in male Harmostini (Rhopalidae), is described for the first time. Some stridulatory mechanisms appear to be non-homoplastic apomorphies within Rhopalidae, while others are homoplastic or potentially homoplastic within Coreidae and Alydidae, respectively. We detected no losses of these mechanisms once evolved, suggesting they are adaptive. Our work sets the stage for further behavioural, evolutionary and ecological studies to better understand the context in which these traits evolve and change.

First record of Leptoglossusoccidentalis Heidemann, 1910 (Hemiptera, Coreidae) in the Canary Islands, a novel pine pest detected through citizen science in an oceanic archipelago.

Background: The 'western seed bug', known as Leptoglossusoccidentalis, is considered a global invasive species that has experienced a recent rapid expansion worldwide, becoming an important pest species for coniferous forests. New information: With the 'Canary Islands early-warning network for the detection and intervention of invasive exotic species' (RedEXOS), this species was detected for the first time in the Canarian archipelago in an urban area in the eastern part of the island of Gran Canaria. This early detection is crucial for understanding the potential damage in one of the islands with the highest surface area of natural endemic pine forest.

Proactive classical biological control of Lycorma delicatula (Hemiptera: Fulgoridae) in California (U.S.): Host range testing of Anastatus orientalis (Hymenoptera: Eupelmidae).

Lycorma delicatula (Hemiptera: Fulgoridae), the spotted lanternfly, native to China, invaded and established in the northeast U.S. in 2014. Since this time, populations have grown and spread rapidly, and invasion bridgeheads have been detected in mid-western states (i.e., Indiana in 2021). This invasive pest presents a significant threat to Californian agriculture. Therefore, a proactive classical biological control program using Anastatus orientalis (Hymenoptera: Eupelmidae), a L. delicatula egg parasitoid native to China, was initiated in anticipation of eventual establishment of L. delicatula in California. In support of this proactive approach, the potential host range of A. orientalis was investigated. Eggs of 34 insect species either native or non-native to the southwestern U.S. were assessed for suitability for parasitism and development of A. orientalis. Of the native species tested, 10, 13, and one were Hemiptera, Lepidoptera, and Mantodea, respectively. Of the non-native species, eight Hemiptera and two Lepidoptera were evaluated. Host range tests conducted in a quarantine facility, exposed individually mated A. orientalis females (Haplotype C) to non-target and target (i.e., L. delicatula) eggs in sequential no-choice and static choice experiments to determine suitability for parasitization and development. Additionally, the sex ratio, fertility, and size of offspring obtained from non-target and target eggs were evaluated. Results of host range testing indicated that A. orientalis is likely polyphagous and can successfully parasitize and develop in host species belonging to at least two different orders (i.e., Hemiptera, Lepidoptera) and seven families (Coreidae, Erebidae, Fulgoridae, Lasiocampidae, Pentatomidae, Saturniidae and Sphingidae). Prospects for use of A. orientalis as a classical biological control agent of L. delicatula in the southwestern U.S. are discussed.

Phylogeny of Coreoidea based on mitochondrial genomes show the paraphyly of Coreidae and Alydidae.

Coreoidea (Insecta: Hemiptera: Heteroptera) is a widely distributed and agriculturally important bugs. However, the phylogeny of Coreoidea lacked consensus on higher-level relationships and several studies by comparative morphological characters and molecular data suggested the non-monophyly of two families: Coreidae and Alydidae. The mitochondrial genome (mitogenome) has long been thought to be a significant marker to understand phylogenetic relationships, but the mitogenome in Alydidae is scarce to date. In the present study, we gathered the mitogenomes of 28 species from four families of Coreoidea excluding Hyocephalidae (Alydidae, Coreidae, Rhopalidae, and Stenocephalidae), including four newly sequenced mitogenomes of Alydidae, and conducted mitogenomic organization and phylogenetic studies. We used maximum likelihood and Bayesian inference methods to infer the higher-level phylogeny from the perspective of mitogenomes, primarily to investigate the phylogenetic relationship betweeen Coreidae and Alydidae. We add evidence that neither Alydidae nor Coreidae are monophyletic based on mitogenomes. Newly sequenced mitogenomes of Alydidae have traditional gene structure and gene rearrangement was not found. Alydinae was always recovered as closely related to Pseudophloeinae of the coreid subfamily with high support. The placement of the coreid subfamily Hydarinae and alydid subfamily Micrelytrinae are unstable depending on approach used. In terms of the length and nucleotide composition of the protein coding genes in mitogenomes, Pseudophloeinae and Hydarinae of coreid were more similar to Alydidae. The unsettled classification issues of Coreidae and Alydidae by mitogenomes were demonstrated in this work, indicating that further study is needed.

Distribution of Two Strains of Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae) in the Western Hemisphere: Is L. zonatus a Potential Invasive Species in California?

The leaffooted plant bug, Leptoglossus zonatus (Dallas) (Hemiptera: Coreidae) is polyphagous and widely distributed in the Western Hemisphere. Although it has been recorded in California since around 1900, it has become a more common pest in almonds in the last decade. Other studies have shown that an established insect can become a pest when a new genotype is introduced. This study investigated the distribution of two lineages (strains) of L. zonatus in the Western Hemisphere. Specimens from the Leptoglossus collection in the national insect collection in Mexico were used to extract DNA and sequence the mitochondrial DNA cytochrome oxidase I (mtDNA COI) gene, for use in population genetic and phylogenetic analyses. New sequences from Mexico, Central and South America were combined with those available in GenBank, from California and Brazil. Two lineages (strains) of L. zonatus were uncovered. One lineage occurs in California, Mexico and Ecuador. The second lineage is more widespread and found in California, Mexico, Guatemala, Nicaragua, Bolivia and Brazil. The haplotype number and diversity, and nucleotide diversity, were found for samples from California, Mexico, and Brazil, for the two lineages, and for all 118 sequences combined. All sequences combined produced five haplotypes, and a haplotype diversity of 0.54. California and Brazil had 3 haplotypes each, with one haplotype shared (5 total). Haplotype diversity in California and in Brazil were 0.526 and 0.505, respectively. A haplotype network found that one haplotype was most abundant and widespread. The small number of haplotypes, a range expansion, and economic pest status of L. zonatus in California, all contribute to this insect being a potentially invasive insect pest.

The Importance of Environmentally Acquired Bacterial Symbionts for the Squash Bug (Anasa tristis), a Significant Agricultural Pest.

Most insects maintain associations with microbes that shape their ecology and evolution. Such symbioses have important applied implications when the associated insects are pests or vectors of disease. The squash bug, Anasa tristis (Coreoidea: Coreidae), is a significant pest of human agriculture in its own right and also causes damage to crops due to its capacity to transmit a bacterial plant pathogen. Here, we demonstrate that complete understanding of these insects requires consideration of their association with bacterial symbionts in the family Burkholderiaceae. Isolation and sequencing of bacteria housed in the insects' midgut crypts indicates that these bacteria are consistent and dominant members of the crypt-associated bacterial communities. These symbionts are closely related to Caballeronia spp. associated with other true bugs in the superfamilies Lygaeoidea and Coreoidea. Fitness assays with representative Burkholderiaceae strains indicate that the association can significantly increase survival and decrease development time, though strains do vary in the benefits that they confer to their hosts, with Caballeronia spp. providing the greatest benefit. Experiments designed to assess transmission mode indicate that, unlike many other beneficial insect symbionts, the bacteria are not acquired from parents before or after hatching but are instead acquired from the environment after molting to a later developmental stage. The bacteria do, however, have the capacity to escape adults to be transmitted to later generations, leaving the possibility for a combination of indirect vertical and horizontal transmission.

Trade-offs between weapons and testes do not manifest at high social densities.

Social conditions can alter the allocation of resources to reproductive traits. For example, an increase in social density during development is frequently associated with an increase in the testes mass of males. Sperm competition theory assumes that increased investment in testes should come at the expense of investing into precopulatory traits, such as sexually selected weaponry. However, much remains unknown about the role of the social context on the concurrent, relative investment in both testes and weapons. We found that the leaf-footed cactus bug, Narnia femorata (Hemiptera: Coreidae), grew nearly 20% larger testes when raised in high social densities. In addition to manipulating social density, we used autotomy (limb loss) to limit investment in their hindlimb weapon during development. At low densities, we found that those that lost a weapon during development grew larger testes by adulthood, supporting previous work demonstrating a weapons-testes trade-off. However, at high social densities, males that dropped a hindlimb did not grow larger testes, though testes were already large at this density. These results underscore the importance of the social context to resource allocation patterns within the individual.

Ecological niche modeling (ENM) of Leptoglossus clypealis a new potential global invader: following in the footsteps of Leptoglossus occidentalis?

The introduction of alien species is one of the main problems in conservation. Many successful invaders cause severe economic and ecological damage. Such is the case of Leptoglossus occidentalis, a phytophagous true bug native to North America, which has become a pest in Europe, Asia, Africa and South America. Within the genus, another species whose distributional range is expanding toward the east of North America is Leptoglossus clypealis. As climate determines the successful establishment of insects, the identification of climatically suitable areas for invasive species based on ecological niche models (ENMs) offers an excellent opportunity for preventing invasions. In this study, ENMs were built for both species and their native climatic niches were compared. Their niche breath was also measured. The climatic niches of both species are identical and the niche breadth of L. clypealis is broader than that of L. occidentalis. In view of the great ecological resemblance between these two species, we believe that L. clypealis could became a major pest thus it should be carefully monitored. The results of the present worldwide ENMs showed numerous regions with suitable conditions for the establishment of both species. The future ENMs exhibited a retraction in the suitable areas in North America, Europe and Asia.

Leaf-footed bugs possess multiple hidden contrasting color signals, but only one is associated with increased body size.

Antipredatory displays that incorporate hidden contrasting coloration are found in a variety of different animals. These displays are seen in organisms that have drab coloration at rest, but when disturbed reveal conspicuous coloration. Examples include the bright abdomens of mountain katydids and the colorful underwings of hawk moths. Such hidden displays can function as secondary defenses, enabling evasion of a pursuant predator. To begin to understand why some species have these displays while others do not, we conducted phylogenetic comparative analyses to investigate factors associated with the evolution of hidden contrasting coloration in leaf-footed bugs. First, we investigated whether hidden contrasting coloration was associated with body size because these displays are considered to be more effective in larger organisms. We then investigated whether hidden contrasting coloration was associated with an alternative antipredatory defense, in this case rapid autotomy. We found that leaf-footed bugs with hidden contrasting coloration tended to autotomize more slowly, but this result was not statistically significant. We also found that the presence of a body size association was dependent upon the form of the hidden color display. Leaf-footed bugs that reveal red/orange coloration were the same size, on average, as species without a hidden color display. However, species that reveal white patches on a black background were significantly larger than species without a hidden color display. These results highlight the diversity of forms that hidden contrasting color signal can take, upon which selection may act differently.

Analysis of Holhymenia histrio genome provides insight into the satDNA evolution in an insect with holocentric chromosomes.

Satellite DNAs (satDNA) are fast-evolving repetitive sequences organized in large tandem arrays, with characteristic enrichment in heterochromatin. Knowledge about evolutionary dynamics of this genome fraction is mostly restricted to its characterization in species with monocentric chromosomes, i.e., localized centromeres. In holocentric species, with non-localized centromeres, satDNAs have been largely ignored. Here we advance the understanding of satDNA evolution among holocentric species by characterization of the most abundant satDNAs in the hemipteran Holhymenia histrio, integrating genomic and chromosomal analyses. High plasticity at chromosomal and molecular levels was noticed for 34 satDNAs populating H. histrio genome. One satDNA family in particular (HhiSat01-184) was highly amplified on multiple chromosomes and also highly polymorphic. Our data support the emergence of a new satDNA family from this abundant satDNA, confined to a single chromosome. Moreover, we present new information about composition of a peculiar chromosome in Coreidae, the m-chromosome, and of the X chromosome. Overall, the molecular and chromosomal patterns for satDNAs in the holocentric species H. histrio seem to be similar to those observed in monocentric species.

True bugs living on ant-defended acacias: evasion strategies and ant species preferences, in Costa Rica and Panama / Chinches que viven en acacias defendidas por hormigas: estrategias de evasión y preferencia por especies de hormigas, en Costa Rica y Panamá

Introduction: Herbivores specialized in consuming ant-defended plants evolve strategies to prevent the attack of ant workers. When the plant can associate with more than one ant species, the herbivore evasion strategies may either be species-specific, or flexible enough to successfully deter workers of different ant-plant species. Objectives: We studied the behavior of an herbivore bug (Piezogaster reclusus) on ant-defended acacia trees (Vachellia collinsii), which associates with one of three mutualistic Pseudomyrmex ant species, and report the geographical distribution of the acacia bug species of Costa Rica and Panama. Methods: We tested whether herbivore bugs (1) associate with a particular ant species; (2) use chemical or behavioral strategies to evade the ant workers; (3) adjust the evasion strategy to the ant species living on the acacia tree. We also compared collected acacia bugs with Museum specimens to clarify the identification from Costa Rica and Panama. Results: We found bugs more often on trees with ants, particularly Ps. spinicola, and never on trees with Ps. nigrocinctus. To avoid ant attacks, bugs use evasive behaviors to prevent encounters with the ant workers, that depended on the ant species. Also, indirect evidence of intra and interspecific transfer experiments suggest species-specific chemical camouflage or repellence. We also report an expansion of the Southern limit of Pi. reclusus distribution in Central Panama, and reduced the distribution of Pi. chontalesis to the Chiriquí region. Conclusions: Similar to herbivores specialized on chemically defended plants, herbivores on ant-defended trees could evolve specific mechanisms to deal with the plant defenses. However, plants associated with multiple partners are a challenge to herbivore specialization, and might require behavioral plasticity, as our evidence suggests.

Introducción: Herbívoros especializados en consumir plantas defendidas por hormigas evolucionaron estrategias para prevenir el ataque de las obreras, que pueden ser específicas o flexibles para repeler obreras de diferentes especies. Objetivos: Estudiamos el comportamiento del chinche herbívoro (Piezogaster reclusus), que consume la savia de árboles de acacia, que se pueden asociar con una de tres especies de hormigas mutualistas del género Pseudomyrmex y reportamos el rango geográfico de las especies de chinches de acacias en Costa Rica y Panamá. Métodos: Evaluamos si los chinches herbívoros (1) se asocian preferiblemente con una especie de hormiga; (2) usan estrategias de comportamiento para evadir a las obreras; (3) ajustan su estrategia a la especie de hormiga residente en la acacia. También, comparamos especímenes de los chinches con especímenes de museos, para clarificar la identificación en Costa Rica y Panamá. Resultados: Los chinches fueronmás frecuentes en árboles con hormigas, especialmente Ps. spinicola, y nunca estuvieron en árboles con Ps. nigrocinctus. Los chinches mostraron diferentes comportamientos evasivos dependiendo de la especie de hormiga para prevenir encuentros con las obreras. También, evidencia indirecta de experimentos de transferencia sugiere que hay camuflaje especie-específico o repelencia. Además, reportamos que el límite de distribución de Pi. reclusus llega al centro de Panamá, mientras que Pi. chontalensis solamente está en la región de Chiriquí. Conclusiones: Igual que los herbívoros se especializan en plantas con defensas químicas, herbívoros en plantas con hormigas pueden evolucionar mecanismos específicos para lidiar con las defensas de las plantas. Sin embargo, plantas que se asocian a múltiples especies de hormigas se vuelven un reto para la especialización del herbívoro, y pueden requerir plasticidad de comportamiento como sugieren nuestros datos.

A revision of the Costa Rican species of Stenoeurilla Brailovsky Barrera (Hemiptera: Heteroptera: Coreidae: Stenoscelideini), with the description of two new species, new distributional records, synonymical note, and key to the known species.

The genus Stenoeurilla Brailovsky Barrera (Coreidae) in Costa Rica is revised. Two new species, S. herediana, and S. mesoamericana, are described. New distributional records for S. hansoni are added. A key to the known species of the genus is included. Photographs of dorsal habitus, male genital capsule and parameres are provided as well as drawings of hind tibiae. Stenoscelidea prolixa Brailovsky 1983 is placed in synonymy under Stenoeurilla aenescens (Stål) 1870.

The genus Ctenomelynthus (Hemiptera: Heteroptera: Coreidae: Acanthocephalini), with the description of three new species and key to the known species.

The genus Ctenomelynthus Breddin (1903) is redescribed, and three new species: C. sanchezi from French Guiana, and Venezuela, C. urbinus from Brazil, and C. venustulus from Suriname are described. Ctenomelynthus willineri (Kormilev, 1952), is synonymized under C. coxalis Breddin, 1903. One species, C. bridarollii (Kormilev) is designated as a nomen dubium. New distributional records for C. brunneiventris Breddin, C. coxalis Breddin, and C. inermibus (Distant) are included. Dorsal and ventral photographs and parameres of some species are included. A key to the six known species is given.

Uncovering the molecular organization of unusual highly scattered 5S rDNA: The case of Chariesterus armatus (Heteroptera).

One cluster of 5S rDNA per haploid genome is the most common pattern among Heteroptera. However, in Chariesterus armatus, highly scattered signals were noticed. We isolated and characterized the entire 5S rDNA unit of C. armatus aiming to a deeper knowledge of molecular organization of the 5S rDNA among Heteroptera and to understand possible causes and consequences of 5S rDNA chromosomal spreading. For a comparative analysis, we performed the same approach in Holymenia histrio with 5S rDNA restricted to one bivalent. Multiple 5S rDNA variants were observed in both species, though they were more variable in C. armatus, with some of variants corresponding to pseudogenes. These pseudogenes suggest birth-and-death mechanism, though homogenization was also observed (concerted evolution), indicating evolution through mixed model. Association between transposable elements and 5S rDNA was not observed, suggesting spreading of 5S rDNA through other mechanisms, like ectopic recombination. Scattered organization is a rare example for 5S rDNA, and such organization in C. armatus genome could have led to the high diversification of sequences favoring their pseudogenization.

Cut your losses: self-amputation of injured limbs increases survival.

Autotomy, self-induced limb loss, is an extreme trait observed throughout the animal kingdom; lizards drop their tails, crickets release their legs, and crabs drop their claws. These repeated evolutionary origins suggest that autotomy is adaptive. Yet, we do not have a firm understanding of the selective pressures that promote and maintain this extreme trait. Although multiple adaptive hypotheses exist, research has generally focused on autotomy's adaptive value as a form of predator escape. However, autotomy could also be selected to reduce the cost of an injured limb, which we investigate here. Previously, this alternative hypothesis has been challenging to directly test because when an injury occurs on an autotomizable limb, that limb is almost always dropped (i.e., autotomy is behaviorally fixed within populations). Recently, however, we have identified a species, Narnia femorata (Insecta: Hemiptera: Coreidae), where some individuals autotomize limbs in response to injury, but some do not. This natural variation allowed us to investigate both the survival costs of retaining an injured limb and the benefits of autotomizing it. In this study, we find a positive association between autotomizing injured limbs and survival, thereby quantifying a new and likely widespread benefit of autotomy-reducing the cost of injury.

A new species of Physomerus Burmeister (Hemiptera: Heteroptera: Coreidae: Coreinae), with a key to the species of India.

A new species from India, Physomerus centralis sp. nov. (Hemiptera: Heteroptera: Coreidae) is described and illustrated with both male and female genitalia. Morphological measurements and their ratios were taken as additional diagnostic characters. A key to the Indian species of the genus Physomerus Burmeister is provided.