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Review of secondary reproduction in termites (Insecta: Isoptera) with comments on its role in termite ecology and social evolution
Abstract
This review assembles records of neotenic reproductives in 199 species in 61 genera in 6 families and adultoid reproductives in 35 species In 14 genera in 2 families of in the order Isoptera. Neotenic reproductives are reported for 61.7% of lower termite genera, but for only 13.4% of higher termite genera (Termitidae). Secondary reproduction is assessed in relation to the following nine termite ecotypes: 1) dry endoxylophagy, 2) damp endoxylophagy, 3) xylophagous foraging, 4) arborealxylophagy, 5) epigeous nesting, 6) mound building, 7) humivory, 8) grass and litter feeding, and 9) nest inquilinism. Neotenics appear to be common in termites that occupy all xylophagous ecotypes, but rare or obsolete in mound building and humivorous termites. Hypotheses concerning the role of neotenic reproduction in termite social evolution are discussed. Cross taxa comparisons show that facultative neoteny is a primitive element in termite caste systems, supporting the hypothesis that neotenics evolved as the first physical caste in termites due to individual-level selection forces associated with the primitive endoxylophagous ecotype. The origin of the neotenic caste would have introduced a reproductive alternative to alate development, and thus provided a direct-fitness component to the fitness outlook of nondispersing colony members. This potential for reproduction without dispersal would have reduced the fitness cost of not dispersing, and thereby may have promoted selection for further diversification of termite caste potentialities as pseudergates and reproductive soldiers. Thus, it is concluded that neotenic reproduction was an important enabling mechanism in the early eusocial evolution of termites. Neotenic reproduction has evolved as a less prominent feature of the biology of most higher termites and has been lost and replaced by adultoid replacement reproduction in the Macrotermitinae, and in other groups among the Termitidae. Adultoids appear to be selected over neotenics in taxa with a stable food base, centralized nesting, secure royal cells, and highly physogastric primary queens.
... However, secondary reproductives within the Termitidae can develop from the nymphal line (alates). These are termed 'adultoids', refering to alates that shed their wings and reproduce within their natal colony (Noirot 1969(Noirot , 1990Myles 1999;Korb and Hartfelder 2008). Korb and Hartfelder (2008) suggested that adultoids are not neotenic, but are in fact imagoes. ...
... Moreover, FFR individuals retain some immature characteristics (light pigmentation with slight sclerotisation). They are unable to fly in spite of having wings, which are morphologically similar to those of the adultoids of pseudoimagoes or microimagoes in other termite species (Roisin and Pasteels 1985;Myles 1999). ...
Three types of replacement reproductives exist within termite colonies: nymphoids developed from nymphs, ergatoids from workers, and adultoids from alates. To date, the only two types of replacement reproductives described in Reticulitermes are nymphoids and ergatoids. We found that in addition to alates, the sixth stage nymphs (N6 nymphs) of R. labralis could also undergo eclosion and become one of two secondary reproductive types: (1) nymphoids or (2) floppy wing form reproductives (FFR). The FFRs would become replacement reproductives within their natal colony after wing shedding. These reproductives have a light pigmentation, with slight sclerotization of their floppy wings, and are capable of producing offspring within their natal colony. FFRs differed in morphology to the alates after eclosion. We found that oogenesis had completed yolk accumulation and reached the vitellogenesis stage in alates. By contrast, the vitellogenic oocytes were absent at the end of ovarioles in FFRs, nymphoids, and N6 nymphs, showing that oogenesis did not reach the vitellogenesis stage. In other words, the ovarian status of FFRs would more likely resemble nymphoids rather than primary reproductives. Microsatellite analyses of four loci indicated that FFR individuals , workers, and alates were all produced by sexual reproduction. Thus, FFRs can be classified as another type of secondary reproductives in addition to the nymphoid and ergatoid morphs in R. labralis. The R. labralis FFR is similar to the adultoids in higher termites except for its larval characteristics, which adds to the evidence that R. labralis is a transitional species between the lower and higher termite.
... To process the data, we rounded the maximum colony size values to the nearest power of 10 and then applied the logarithm base 10 function to them. Much of the data on sterility was also previously acquired from studies compiling developmental plasticity and worker fertility data across the termites [37,46]. We define obligate sterility as a species which has workers unable to take over the colony or found their own under any circumstances (box 1). ...
... Functional sterility is defined as species which have workers able to become reproductives only under extreme circumstances, for instance where the primary reproductives have died (box 1). There are varying levels of reliability with the data, as some are long-term observational data stating that no replacement reproductive were present, some were field-based colony orphaning experiments and others laboratory-based colony orphaning [37,46]. We can only be totally certain that a species has actual obligate sterility when doing these in-depth colony orphaning experiments. ...
Sociality underpins major evolutionary transitions and significantly influences the structure and function of complex ecosystems. Social insects, seen as the pinnacle of sociality, have traits like obligate sterility that are considered ‘master traits’, used as single phenotypic measures of this complexity. However, evidence is mounting that completely aligning both phenotypic and evolutionary social complexity, and having obligate sterility central to both, is erroneous. We hypothesize that obligate and functional sterility are insufficient in explaining the diversity of phenotypic social complexity in social insects. To test this, we explore the relative importance of these sterility traits in an understudied but diverse taxon: the termites. We compile the largest termite social complexity dataset to date, using specimen and literature data. We find that although functional and obligate sterility explain a significant proportion of variance, neither trait is an adequate singular proxy for the phenotypic social complexity of termites. Further, we show both traits have only a weak association with the other social complexity traits within termites. These findings have ramifications for our general comprehension of the frameworks of phenotypic and evolutionary social complexity, and their relationship with sterility.
... Neotenics are found in many termite families (Myles, 1999;Roisin, 1999). These neotenic forms appear in termite colonies and take over the reproductive function to maintain the colonies when the primary reproductive individuals die. ...
Reproductive systems of termite colonies may involve the number of individuals in the reproductive caste and the copulatory selectivity of reproductive individuals (i.e., polyandry or polygamy), both of them impacting directly the fertility and genetic diversity of the colony. Polygamy is widespread in the lower termites, whereas polyandry appears to be mostly absent in termites. In this paper, the differentiation of male and female neotenics was observed in orphaned experimental colonies of the subterranean termite Reticulitermes labralis. The artificial orphaned colonies began to produce neotenics only a week after colony establishing, with more neotenics appearing in the same group as time went by. Finally, each experimental group reserved multi-neotenics consisting of male and female neotenic individuals. Our results demonstrated that these neotenic individuals retained in the colony participated in reproduction. A genetic analysis at four microsatellite loci showed that in addition to the conspicuous morphologically male reproductives, there were inconspicuous males or workers that had copulated with the females in the orphaned colony. Multiple male and female reproductive individuals existed together in a single colony, and one female neotenic could mate with several male reproductives in a short time. Thus, multiple male and female reproductive systems and a polyandric mating system are present in R. labralis.
... 2023). Neoteny being frequent in the Heterotermitidae (Coptotermes + Heterotermes + Reticulitermes) 55 , we postulate that competition among neotenics and split sex ratios are common in this clade. ...
Termites are eusocial cockroaches whose altruist caste is constituted of males and females. While sex ratio theory predicts a balanced investment between sexes in diploid organisms, extreme deviations are observed in termites, both in altruists and alate reproductives. Here, we expand the theoretical framework for the prediction of alate population sex ratio by considering partitioned sexual and parthenogenetic reproduction, and female/male relatedness asymmetries arising from their sex-linked chromosome complexes. We consider the viewpoint of either the primary reproductives or the altruists while accounting for the effect of caste developmental systems on the sex ratio. We compile all data on alate sex ratios available to date (97 species), and found the direction of the sex ratio bias to be consistent within major taxonomic groups. We test our models, along with models of intrasexual competition, on an exploratory set of 13 species with available demographic data. Our analyses indicate that the factors explaining bias in alate sex ratio are variable and include sexual dimorphism, sex-asymmetric inbreeding, imperfect use of sexual and parthenogenetic reproduction, sex-linked genomic inheritance, intrasexual competition and caste developmental constraints. Our study provides an integrative framework for sex ratio and conflicts in termites, and closes in on a universal theory.
... The conventional sexual mechanism of fertilized eggs is used by termites to develop heterozygous workers, nymphs, and alates, whereas new neotenic queens develop as ergatoids, nymphoids, and adultoids. They take over natal colonies as replacement reproductives when the primary reproductives weaken or die, particularly in the Termitidae, Kalotermitidae, and Rhinotermitidae (da Silva and Haifig, 2020;Korb and Hartfelder, 2008;Myles, 1999;Su et al., 2015;Wu et al., 2024). This unusual reproductive system allows social insect queens to maintain appropriate genetic diversity in workers, while exploiting their genetic contribution to future queens (Pearcy et al., 2004). ...
Asexual queen succession (AQS) species produce queens via thelytokous parthenogenesis, which significantly impacts their social life history. For the first time, we discovered that Reticulitermes aculabialis exhibits the phenomenon of parthenogenesis under experimental conditions, and we also investigated the genetic structure of wild colonies of this species using polymorphic microsatellite loci. Our genetic analysis revealed that 93.2% of the secondary queens in the wild colonies were homozygous at all loci, indicating parthenogenesis in these secondary queens, while workers (2.5%), soldiers (0%), nymphs (0%), and alates (6.7%) had low rates. Genetic analysis revealed that the mean number of alleles per group (Na) ranged from 2.000 ± 0.000 to 2.500 ± 0.428, with 83.3% polymorphic loci (PPL). The observed heterozygosity (Ho) varied from 0.467 ± 0.141 to 0.583 ± 0.098, indicating significant genetic diversity among workers and soldiers. In contrast, soldiers and nymph develop predominantly through sexual reproduction than alates and workers. The occurrence of AQS in R. aculabialis suggests a different mechanism of ploidy restoration, highlighting the diversity of reproductive mechanisms across various lineages of the Termitidae and non-Termitidae termites.
... However, certain species can produce secondary neotenic reproductives (derived from nymph tor worker termites) to replace aging primary or previous secondary reproductives, thus potentially prolonging colony lifespan indefinitely if secondary reproductives are continuously produced (Matsuura et al. 2009). Secondary reproductives are prevalent in 61.7% of lower termite genera (e.g., Reticulitermes and Coptotermes in our study), but only in 13.4% of higher termite genera (Termitidae) (Myles 1999). Macrotermes and Odontotermes, as two of fungus-growing Termitidae genera, are unable to produce secondary reproductives, thereby relying solely on the maximum lifespan of primary reproductives, estimated at a maximum of 20 years (Wisselink et al. 2020). ...
Context
Abiotic filtering, including environmental and dispersal filtering, is frequently observed resulting in reduced diversity and more similar species assemblages following habitat fragmentation. Nonetheless, the significance of competitive exclusion is often underestimated.
Objectives
We investigated the dominant assembly process among termite communities on land-bridge islands, focusing on species known for their high territoriality. We hypothesized that competitively superior species tend to dominate more favorable habitats, such as larger and less isolated islands. Consequently, we anticipated lower diversity and greater similarity in species assemblages than would be expected.
Methods
Termite communities were surveyed using standardized transects on 24 islands. We quantified the standardized effects of island area and isolation on taxonomic, phylogenetic and functional diversity by comparing observed patterns with randomly generated communities (i.e., stochastic process). A phylogenetic generalized linear mixed model (PGLMM) was conducted to examine species-specific responses to environmental factors and competition intensity (i.e., heterospecific abundance).
Results
We found that taxonomic, phylogenetic and functional diversity were lower than expected on larger and less isolated islands, suggesting that competitive exclusion was the dominant mechanism shaping termite communities in TIL. PGLMM showed that two fungus-growing species with larger body sizes increased with competition intensity, while other species exhibited negative responses. Notably, the abundance of fungus-growing species showed sharper increase with island area and decrease with isolation compared to other feeding groups. These findings demonstrate that competitively superior species prefer high-quality habitats and are more sensitive to habitat fragmentation.
Conclusions
Our study highlights the significance of competitive exclusion in shaping termite communities and emphasizes the need to consider both competitive and niche difference among species or functional groups when predict changes in community structure and biodiversity loss resulting from habitat fragmentation.
In 1995, the launch of the first commercial chitin synthesis inhibitor (CSI) bait led to the transformation of the subterranean termite control industry around the world. Their slow mode of action, which relies on both their ability to be transferred among nestmates and termite molting biology, has made them cost-effective solutions for subterranean termite colony elimination while minimizing the introduction of pesticides into the soil toward an environmentally sustainable strategy. However, despite successful commercial implementations, the acceptance of their use varies within the pest control industry around the world. Notably, the nuanced complexity of how CSI baits lead to colony elimination upon feeding by termite foragers has, in part, remained elusive for the past 3 decades, allowing for long-lasting misconceptions to persist. A recent series of studies has since provided complementary elements of understanding how CSI baits utilize termites’ inherent colony demography, behavior, and physiology to trigger colony elimination after a characteristic succession of events within the colony collapse process. I here provide a synthetic overview of subterranean termite colony characteristics when exposed to CSI baits using Coptotermes (Wasmann) (Blattodea: Heterotermitidae) as a primary model system. The changes in colony demography through the colony collapse reflect how the mode of action of CSI baits makes them a prime solution for sustainable subterranean termite pest management. Following decades of innovation, ongoing interactions among termite researchers, bait product manufacturers, and pest management providers must continue to bring solutions to existing and emerging termite pest problems around the world.
Invasive drywood termites are one of the most challenging species to detect in the early invasion process as they can infest a small piece of wood and be transported by human activity. Cryptotermes domesticus (Haviland, 1898) is native to south Asia and Australia and has been introduced into many other Asian countries and pacific islands, where they cause damage to furniture and wooden structures. Recently, an established colony of C. domesticus has been found in the Seoul metropolitan area, Republic of Korea, where drywood termites were not thought to be able to establish due to low winter temperatures. The discovery of C. domesticus was initiated from a post on an internet forum in which an anonymous homeowner collected alates in an apartment and asked for pest identification. This information was readily delivered to professional entomologists, and a task force was formed for inspection. During the thorough inspection, an infested sliding door frame was identified and a colony of C. domesticus was found. Instead of fumigation and localized pesticide treatment, the door and frame were removed and replaced, which was the most cost-effective control measure as the colony was only found there. Since the potential spread of C. domesticus is uncertain, the task force collaborated with the media, including newspapers and broadcasting news, to disseminate information to help recognize any additional unreported infestations. This study provides insights on how to cooperate with the media and citizens when a new invasive species is found.
Investment into neural tissue is expected to reflect the specific sensory and behavioral capabilities of a particular organism. Termites are eusocial insects that exhibit a caste system in which individuals can develop into one of several morphologically and behaviorally distinct castes. However, it is unclear to what extent these differences between castes are reflected in the anatomy of the brain. To address this question, we used deformation-based morphometry to conduct pairwise comparisons between the brains of different castes in the eastern subterranean termite, Reticulitermes flavipes. Workers exhibited enlargement in the antennal lobes and mushroom bodies, while reproductives showed increased investment into the optic lobes and central body. In addition, caste-specific enlargement was observed in regions that could not be mapped to distinct neuropils, most notably in soldiers. These findings demonstrate a significant influence of caste development on brain anatomy in termites alongside convergence with eusocial hymenopteran systems.
Three families, 5 genera and 7 species of termites were found in the Krakatau Islands. Between 1908-1982, 2 species seem to have been replaced by other congeneric species in Rakata Besar, the largest island of the group. Termites in the islands were characterized taxonomically by the dominance of lower termites (Kalotermitidae and Rhinotermitidae) and ecologically by wood feeders constructing their nests in the wood itself, whereas those of the mainland (W Java) were characterized taxonomically by the dominance of higher termites (Termitidae) and ecologically by wood or humus feeders constructing their nests in the soil. The importance of dispersal ability by rafting and asymmetrical interspecific competition is discussed in an attempt to explain the presence or absence of termite groups with different life types in the islands.-from Author