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The higher classification of termites requires substantial revision as the Neoisoptera, the most diverse termite lineage, comprise many paraphyletic and polyphyletic higher taxa. Here, we produce an updated termite classification using genomic-scale analyses. We reconstruct phylogenies under diverse substitution models with ultraconserved elements analyzed as concatenated matrices or within the multi-species coalescence framework. Our classification is further supported by analyses controlling for rogue loci and taxa, and topological tests. We show that the Neoisoptera are composed of seven family-level monophyletic lineages, including the Heterotermitidae Froggatt, Psammotermitidae Holmgren, and Termitogetonidae Holmgren, raised from subfamilial rank. The species-rich Termitidae are composed of 18 subfamily-level monophyletic lineages, including the new subfamilies Crepititermitinae, Cylindrotermitinae, Forficulitermitinae, Neocapritermitinae, Protohamitermitinae, and Promirotermitinae; and the revived Amitermitinae Kemner, Microcerotermitinae Holmgren, and Mirocapritermitinae Kemner. Building an updated taxonomic classification on the foundation of unambiguously supported monophyletic lineages makes it highly resilient to potential destabilization caused by the future availability of novel phylogenetic markers and methods. The taxonomic stability is further guaranteed by the modularity of the new termite classification, designed to accommodate as-yet undescribed species with uncertain affinities to the herein delimited monophyletic lineages in the form of new families or subfamilies., (© 2024. The Author(s).)

With recent evidence of hybridization events in the field, the phenotypic traits of F1 hybrid colonies of 2 destructive subterranean termite species, Coptotermes formosanus Shiraki and Coptotermes gestroi (Wasmann) remain to be investigated. In this study, laboratory colonies of 2 conspecific pairings and 2 heterospecific pairings (hybrid F = ♀C. formosanus × ♂C. gestroi, hybrid G = ♀C. gestroi × ♂C. formosanus) were examined in Florida, USA, and in Taiwan. Colony nest architecture for both hybrids displayed disorganized carton materials compared to the defined trabecular carton of both parental species. Soldier head measurements were not a reliable approach for diagnostic purposes, as soldier morphometric traits widely overlapped across all mating combinations, except for hybrid F soldiers displaying abnormally long mandibles. Hybrid F soldiers' mandibles also remained parallel when at rest. However, 4 qualitative morphological differences in soldiers were determined for diagnostic purposes. First, the fontanelle in both hybrids is horizontally ellipsoid whereas subcircular in C. gestroi and trianguliform in C. formosanus. Second, sclerotized striations along the postmental sulcus are present in C. gestroi, absent in C. formosanus, and intermediate in both hybrid soldier types. Third, each lateral margin of the fontanelle is flanked by 2 setae in C. formosanus and both hybrids, while a single seta resides on each side of the fontanelle in C. gestroi. Finally, C. gestroi and hybrid soldiers' heads are characterized by a bulging vertex that is lacking in C. formosanus. Therefore, a combination of these 4 characteristics now allows for soldier identification of hybrid Coptotermes., (© The Author(s) 2023. Published by Oxford University Press on behalf of Entomological Society of America.)

Perfume making in male orchid bees is a unique behavior that has given rise to an entire pollination syndrome in the neotropics. 1 , 2 Male orchid bees concoct and store species-specific perfume mixtures in specialized hind-leg pockets 3 using volatiles acquired from multiple environmental sources, including orchid flowers. 4 , 5 However, the function and the ultimate causes of this behavior have remained elusive. 2 , 6 Although previous observations suggested that male perfumes serve as chemical signals, the attractiveness for females has not be shown. 7 , 8 Here, we demonstrate that the possession of perfume increases male mating success and paternity in Euglossa dilemma, a species of orchid bees recently naturalized in Florida. We supplemented males reared from trap-nests with perfume loads harvested from wild conspecifics. In dual-choice experiments, males supplemented with perfumes mated with more females, and sired more offspring, than untreated, equal-aged, control males. Although perfume supplementation had little effect on the intensity of male courtship display, it changed the dynamics of male-male interactions. Our results demonstrate that male-acquired perfumes are sexual signals that stimulate females for mating and suggest that sexual selection is key in shaping the evolution of perfume communication in orchid bees., Competing Interests: Declaration of interests The authors declare no competing interests., (Copyright © 2023 Elsevier Inc. All rights reserved.)

Nitrogen, a limiting growth factor in wood-feeding insects, was hypothesized to play a role in the recently discovered behavior of subterranean termites returning to the nest to molt. Coptotermes gestroi (Wasmann) exuviae is approximately 11% N by dry weight, and therefore a potentially rich source of recyclable nitrogen. Exuviae from a C. gestroi colony were marked with immunoglobulin G (IgG) and were fed to two-year-old C. gestroi colonies. IgG-marked exuviae were detected with an enzyme-linked immunosorbent assay. The IgG marker was later detected in every caste and life stage except first-instar larvae (L1). The proportion of individuals positive for the marker varied by caste, with the queens always being positive for the marker. The queens and second-or-higher-instar workers (W2+) had significantly higher concentrations of the marker than the eggs and L1. The trophic path of exuviae includes individuals that directly fed on marked exuviae (workers and possibly second-instar larvae) and individuals that secondarily received marked exuviae through trophallaxis (queens, kings, and soldiers). This study described the trophic path of consumed exuviae and demonstrated its role in the recycling of nitrogen in a subterranean termite. Molting at the central nest may be an efficient means to transfer nitrogen from shed exuviae to recipients and may be a nitrogen recycling behavior conserved from a termite ancestor., (© The Author(s) 2023. Published by Oxford University Press on behalf of Entomological Society of America.)

Termites (Blattodea: Isoptera) have evolved specialized defensive strategies for colony protection. Alarm communication enables workers to escape threats while soldiers are recruited to the source of disturbance. Here, we study the vibroacoustic and chemical alarm communication in the wood roach Cryptocercus and in 20 termite species including seven of the nine termite families, all life-types, and all feeding and nesting habits. Our multidisciplinary approach shows that vibratory alarm signals represent an ethological synapomorphy of termites and Cryptocercus. In contrast, chemical alarms have evolved independently in several cockroach groups and at least twice in termites. Vibroacoustic alarm signaling patterns are the most complex in Neoisoptera, in which they are often combined with chemical signals. The alarm characters correlate to phylogenetic position, food type and hardness, foraging area size, and nesting habits. Overall, species of Neoisoptera have developed the most sophisticated communication system amongst termites, potentially contributing to their ecological success., (© 2023. The Author(s).)

Elaborate task allocation is key to the ecological success of eusocial insects. Termite colonies are known for exhibiting age polyethism, with older instars more likely to depart the reproductive center to access food. However, it remains unknown how termites retain this spatial structure against external disturbances. Here we show that a subterranean termite Coptotermes formosanus Shiraki combines age polyethism and behavioral flexibility to maintain a constant worker proportion at the food area. Since this termite inhabits multiple wood pieces by connecting them through underground tunnels, disastrous colony splitting events can result in the loss of colony members. We simulated this via weekly removal of all individuals at the food area. Our results showed that termites maintained a worker proportion of ~ 20% at the food area regardless of changes in total colony size and demographic composition, where younger workers replaced food acquisition functions to maintain a constant worker proportion at the food area. Food consumption analysis revealed that the per-capita food consumption rate decreased with younger workers, but the colony did not compensate for the deficiency by increasing the proportion of workers at the feeding site. These results suggest that termite colonies prioritize risk management of colony fragmentation while maintaining suitable food acquisition efficiency with the next available workers in the colony, highlighting the importance of task allocation for colony resiliency under fluctuating environments., (© 2022. The Author(s).)

Background: Foraging in group living animals such as social insects, is collectively performed by individuals. However, our understanding on foraging behavior of subterranean termites is extremely limited, as the process of foraging in the field is mostly concealed. Because of this limitation, foraging behaviors of subterranean termites were indirectly investigated in the laboratory through tunnel geometry analysis and observations on tunneling behaviors. In this study, we tracked subsets of foraging workers from juvenile colonies of Coptotermes formosanus (2-yr-old) to describe general foraging behavioral sequences and to find how foraging workers allocate time between the foraging site (food acquisition or processing) and non-foraging site (food transportation)., Results: Once workers entered into the foraging site, they spent, on average, a significantly longer time at the foraging site than the non-foraging site. Our clustering analysis revealed two different types of foraging workers in the subterranean termite based on the duration of time they spent at the foraging site and their foraging frequency. After entering the foraging site, some workers (cluster 1) immediately initiated masticating wood fragments, which they transferred as food boluses to recipient workers at the foraging site. Conversely, the recipient workers (cluster 2) moved around after entering the foraging site and received food from donating workers., Conclusions: This study provides evidence of task specialization within foraging cohorts in subterranean termites., (© 2021. The Author(s).)

Intrinsic dinitrogen (N 2 ) fixation by diazotrophic bacteria in termite hindguts has been considered an important pathway for nitrogen acquisition in termites. However, studies that supported this claim focused on measuring instant N 2 fixation rates and failed to address their relationship with termite colony growth and reproduction over time. We here argue that not all wood-feeding termites rely on symbiotic diazotrophic bacteria for colony growth. The present study looks at dietary nitrogen acquisition in a subterranean termite (Rhinotermitidae, Coptotermes). Young termite colonies reared with wood and nitrogen-rich organic soil developed faster, compared to those reared on wood and inorganic sand. More critically, further colony development was arrested if access to organic soil was removed. In addition, no difference of relative nitrogenase expression rates was found when comparing the hindguts of termites reared between the two conditions. We therefore propose that subterranean termite (Rhinotermitidae) colony growth is no longer restricted to metabolically expensive intrinsic N 2 fixation, as the relationship between diazotrophic bacteria and subterranean termites may primarily be trophic rather than symbiotic. Such reliance of Rhinotermitidae on soil microbial decomposition activity for optimal colony growth may also have had a critical mechanistic role in the initial emergence of Termitidae., (© 2021. The Author(s).)

In collective animal motion, coordination is often achieved by feedback between leaders and followers. For stable coordination, a leader's signals and a follower's responses are hypothesized to be attuned to each other. However, their roles are difficult to disentangle in species with highly coordinated movements, hiding potential diversity of behavioural mechanisms for collective behaviour. Here, we show that two Coptotermes termite species achieve a similar level of coordination via distinct sets of complementary leader-follower interactions. Even though C. gestroi females produce less pheromone than C. formosanus , tandem runs of both species were stable. Heterospecific pairs with C. gestroi males were also stable, but not those with C. formosanus males. We attributed this to the males' adaptation to the conspecific females; C. gestroi males have a unique capacity to follow females with small amounts of pheromone, while C. formosanus males reject C. gestroi females as unsuitable but are competitive over females with large amounts of pheromone. An information-theoretic analysis supported this conclusion by detecting information flow from female to male only in stable tandems. Our study highlights cryptic interspecific variation in movement coordination, a source of novelty for the evolution of social interactions.

Subterranean termites are hemimetabolous social insects where most of the individuals in a colony molt on a regular basis until they die. Nitrogen is a limiting growth factor in wood-feeding insects, such as termites. Because the exuviae of molting termites are consumed by nestmates, it is possible that exuviae represent a potential source of nitrogen that could be recycled and be part of the overall nitrogen conservation strategy of the colony. Although it was documented that cockroach exuviae can contain relatively high levels of nitrogen, the nitrogen content of subterranean termite exuviae has not been examined. This study determines the nitrogen content of Coptotermes gestroi (Wasmann) exuviae collected from four-year-old laboratory colonies using a carbon/nitrogen analyzer. Coptotermes gestroi exuviae contained 11.24 ± 0.64% N (Mean ± SD). The exuviae had a higher proportion of nitrogen than whole bodies of termites (~10.46%), wood (~0.12%), and organic soil (~2.49%). These results support the importance of exuviae consumption by nestmates during the ecdysis process as an aspect of nitrogen conservation strategies in Coptotermes colonies., Competing Interests: The authors declare no conflict of interest.

Termites are a clade of eusocial wood-feeding roaches with > 3000 described species. Eusociality emerged ~ 150 million years ago in the ancestor of modern termites, which, since then, have acquired and sometimes lost a series of adaptive traits defining of their evolution. Termites primarily feed on wood, and digest cellulose in association with their obligatory nutritional mutualistic gut microbes. Recent advances in our understanding of termite phylogenetic relationships have served to provide a tentative timeline for the emergence of innovative traits and their consequences on the ecological success of termites. While all "lower" termites rely on cellulolytic protists to digest wood, "higher" termites (Termitidae), which comprise ~ 70% of termite species, do not rely on protists for digestion. The loss of protists in Termitidae was a critical evolutionary step that fostered the emergence of novel traits, resulting in a diversification of morphology, diets, and niches to an extent unattained by "lower" termites. However, the mechanisms that led to the initial loss of protists and the succession of events that took place in the termite gut remain speculative. In this review, we provide an overview of the key innovative traits acquired by termites during their evolution, which ultimately set the stage for the emergence of "higher" termites. We then discuss two hypotheses concerning the loss of protists in Termitidae, either through an externalization of the digestion or a dietary transition. Finally, we argue that many aspects of termite evolution remain speculative, as most termite biological diversity and evolutionary trajectories have yet to be explored.

Native to eastern Asia, the Formosan subterranean termite Coptotermes formosanus (Shiraki) is recognized as one of the 100 worst invasive pests in the world, with established populations in Japan, Hawaii and the southeastern United States. Despite its importance, the native source(s) of C. formosanus introductions and their invasive pathway out of Asia remain elusive. Using ~22,000 SNPs, we retraced the invasion history of this species through approximate Bayesian computation and assessed the consequences of the invasion on its genetic patterns and demography. We show a complex invasion history, where an initial introduction to Hawaii resulted from two distinct introduction events from eastern Asia and the Hong Kong region. The admixed Hawaiian population subsequently served as the source, through a bridgehead, for one introduction to the southeastern US. A separate introduction event from southcentral China subsequently occurred in Florida showing admixture with the first introduction. Overall, these findings further reinforce the pivotal role of bridgeheads in shaping species distributions in the Anthropocene and illustrate that the global distribution of C. formosanus has been shaped by multiple introductions out of China, which may have prevented and possibly reversed the loss of genetic diversity within its invasive range.

Cuticular hydrocarbons (CHCs) have, in insects, important physiological and ecological functions, such as protection against desiccation and as semiochemicals in social taxa, including termites. CHCs are, in termites, known to vary qualitatively and/or quantitatively among species, populations, castes, or seasons. Changes to hydrocarbon profile composition have been linked to varying degrees of aggression between termite colonies, although the variability of results among studies suggests that additional factors might have been involved. One source of such variability may be colony age, as termite colony demographics significantly change over time, with different caste and instar compositions throughout the life of the colony. We here hypothesize that the intracolonial chemical profile heterogeneity would be high in incipient termite colonies but would homogenize over time as a colony ages and accumulates older workers in improved homeostatic conditions. We studied caste-specific patterns of CHC profiles in Coptotermes gestroi colonies of four different age classes (6, 18, 30, and 42 months). The CHC profiles were variable among castes in the youngest colonies, but progressively converged toward a colony-wide homogenized chemical profile. Young colonies had a less-defined CHC identity, which implies a potentially high acceptance threshold for non-nestmates conspecifics in young colonies. Our results also suggest that there was no selective pressure for an early-defined colony CHC profile to evolve in termites, potentially allowing an incipient colony to merge nonagonistically with another conspecific incipient colony, with both colonies indirectly and passively avoiding mutual destruction as a result., Competing Interests: None Declared., (© 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.)

Termites have a unique ability to effectively digest lignocellulose with the help of mutualistic symbionts. While gut bacteria and protozoa have been relatively well characterized in termites, the virome remains largely unexplored. Here, we report two genomes of microviruses (termite-associated microvirus-1 [TaMV-1] and termite-associated microvirus-2 [TaMV-2]) associated with the gut of Coptotermes formosanus ., (Copyright © 2019 Schmidlin et al.)

The Asian subterranean termite, Coptotermes gestroi , is a tropical species but has increasingly been collected from the subtropics in recent years, making it sympatric to the Formosan subterranean termite, C. formosanus in at least three areas, Taiwan, Hawaii, and Florida. Simultaneous flights by these two species were observed since 2013 in South Florida, during which interspecies tandems were observed. Laboratory mating of C. formosanus and C. gestroi alates produced hybrid incipient colonies of larger population size. Studies are underway to examine the presence in the field of hybrid colonies in sympatric areas of Taiwan and Florida. Other biological characteristics of C. formosanus × C. gestroi hybrids being studied include temperature tolerance and preference, colony growth rate, wood-consumption rate, and reproductive fertility. This current research aims to determine the potential establishment of a hybrid termite population in south Florida and Taiwan. It investigates the risk of introgressive hybridization in field populations, with an emphasis on its potential ecological, evolutionary, and economic consequences.

While hybridization of an invasive species with a native species is a common occurrence, hybridization between two invasive species is rare. Formosan subterranean termites (Coptotermes formosanus) and Asian subterranean termites (C. gestroi) are both ecologically successful and are the two most economically important termite pests in the world. Both species have spread throughout many areas of the world due to human activity; however, their distributions overlap in only three narrow areas because of distinct ecological requirements. In south Florida, where C. formosanus and C. gestroi are both invasive, the dispersal flight seasons of both species overlapped for the first time on record in 2013 and 2014. Pairings of heterospecific individuals were readily observed in the field and C. gestroi males preferentially engaged in mating behavior with C. formosanus females rather than females from their own species. In the laboratory, heterospecific and conspecific pairings had an equal colony establishment rate, but heterospecific incipient colonies had twice the growth rate of conspecific incipient colonies, suggesting a potential case of hybrid vigor. As all pre-zygotic barriers were lifted between the two species in the field, the apparent absence of post-zygotic barriers in the laboratory raises the possibility for introgressive hybridization in south Florida. While laboratory observations remain to be confirmed in the field, and the alate hybrid fertility is currently unknown, our results raise a tangible concern about the hybridization of two major destructive pest species. Such hybridization would likely be associated with a new economic impact.

Social insect colonies can provide homeostatic conditions that buffer the incidence of environmental fluctuations on individuals, which have contributed to their ecological success. Coptotermes (Isoptera: Rhinotermitidae) is a highly invasive termite genus and several species have important economic impact in many areas of the world. Mature Coptotermes colonies with millions of individuals can provide optimal environmental condition and nurturing capacity for the developing brood. However, it was previously suggested that contrary to mature colonies, incipient colonies may be exposed to critical stress, which may explain for the low success rate of establishment within the first year of the life of a termite colony. We here investigated the stress imposed on individuals of incipient colonies by comparing the developmental instability of individuals between incipient and mature colonies of two Coptotermes species, C. formosanus Shiraki and C. gestroi (Wasmann). We assessed the developmental instability by measuring the asymmetry of morphological traits from the head capsule of the soldier caste. Soldiers from incipient colonies of both species displayed strong asymmetrical traits in comparison to soldiers from mature colonies. We suggest that homeostatic conditions for optimal development are reached as the colony matures, and confirmed that the incipient colony remains a critical bottleneck where individuals are exposed to high developmental stress.

Social insects nesting in soil environments are in constant contact with entomopathogens but have evolved a range of defence mechanisms, resulting in both individual and social immunity that reduce the chance for epizootics in the colony, as in the case of subterranean termites. Coptotermes formosanus uses its faeces as building material for its nest structure that result into a 'carton material', and here, we report that the faecal nest supports the growth of Actinobacteria which provide another level of protection to the social group against entomopathogens. A Streptomyces species with in vivo antimicrobial activity against fungal entomopathogens was isolated from the nest material of multiple termite colonies. Termite groups were exposed to Metarhizium anisopliae, a fungal entomopathogen, during their foraging activity and the presence of Streptomyces within the nest structure provided a significant survival benefit to the termites. Therefore, this report describes a non-nutritional exosymbiosis in a termite, in the form of a defensive mutualism which has emerged from the use of faecal material in the nesting structure of Coptotermes. The association with an Actinobacteria community in the termite faecal material provides an extended disease resistance to the termite group as another level of defence, in addition to their individual and social immunity.

Over the past 50 years, repeated attempts have been made to develop biological control technologies for use against economically important species of subterranean termites, focusing primarily on the use of the entomopathogenic fungus Metarhizium anisopliae. However, no successful field implementation of biological control has been reported. Most previous work has been conducted under the assumption that environmental conditions within termite nests would favor the growth and dispersion of entomopathogenic agents, resulting in an epizootic. Epizootics rely on the ability of the pathogenic microorganism to self-replicate and disperse among the host population. However, our study shows that due to multilevel disease resistance mechanisms, the incidence of an epizootic within a group of termites is unlikely. By exposing groups of 50 termites in planar arenas containing sand particles treated with a range of densities of an entomopathogenic fungus, we were able to quantify behavioral patterns as a function of the death ratios resulting from the fungal exposure. The inability of the fungal pathogen M. anisopliae to complete its life cycle within a Coptotermes formosanus (Isoptera: Rhinotermitidae) group was mainly the result of cannibalism and the burial behavior of the nest mates, even when termite mortality reached up to 75%. Because a subterranean termite colony, as a superorganism, can prevent epizootics of M. anisopliae, the traditional concepts of epizootiology may not apply to this social insect when exposed to fungal pathogens, or other pathogen for which termites have evolved behavioral and physiological means of disrupting their life cycle.