Colony Breeding Structure Research Articles

High numbers of unrelated reproductives in the Australian ‘higher’ termite Nasutitermes exitiosus (Blattodea: Termitidae)

Social insect colonies are among the most complex social organisations in nature, with reproductive and non-reproductive individuals co-ordinating to maintain the survival of the colony. Multiple reproductive schemes occur in social insects, from simple schemes with one founding reproductive pair, to more complex ones involving within-colony inbreeding and more than two unrelated reproductives. Colony breeding schemes and genetic structure remain understudied in termites, compared to the Hymenoptera. In this study, we performed the first genetic characterisation of the colony breeding structure of Nasutitermes exitiosus (Blattodea: Termitidae), an endemic Australian termite with a broad distribution across southern mainland Australia. We analysed the genetic structure of 60 N. exitiosus colonies from the Eastern part of its distribution, using microsatellites and mitochondrial sequence data. We found that most colonies were headed by one founding pair of reproductives, although some colonies exhibited a more complex breeding structure, including within-colony inbreeding and the presence of multiple unrelated reproductives. We found evidence for the presence of seven unrelated queens in one colony, to our knowledge, the highest number of unrelated queens yet found in a termite from the family Termitidae. We found some evidence for genetic isolation by distance, indicating that the species is a relatively poor disperser over long ranges.

Colony Breeding Structure of Reticulitermes (Isoptera: Rhinotermitidae) in Northwest Arkansas

Termites, as social insects, have a complicated life cycle in which the colony breeding structure, that is the number of and origin of reproductives in a colony, can vary in relation to age and environmental factors. In this study, we used genetic methods to characterize the breeding structure of three species of Reticulitermes from three sites in northwest Arkansas and compared two habitats: undeveloped, forested sites and developed, agricultural sites. We found 57.1% of R. flavipes (Kollar) in northwest Arkansas (n = 28) were simple families, 39.3% were extended families and 3.6% were mixed families. Similarly, for R. hageni Banks (n = 23), we found 58.3% simple families, 33.3% extended families, and 8.3% mixed families. All of the R. virginicus (Banks) samples (n = 5) were simple families. For R. flavipes and R. hageni, the percentage of extended families is intermediate to southeastern and northern USA populations, corresponding to the intermediate seasonality and climate in Arkansas. The level of inbreeding in Arkansas, estimated via FIT, was relatively high and similar to northern populations of Reticulitermes. There were significantly more extended family colonies at the developed site compared to the two undeveloped sites which contained more simple family colonies. This difference may occur as a strategy to cope with sparse resources in urban environments or as a consequence of different abiotic factors.

Symbiotic flagellate protists as cryptic drivers of adaptation and invasiveness of the subterranean termite Reticulitermes grassei Clément.

Changes in flagellate protist communities of subterranean termite Reticulitermes grassei across different locations were evaluated following four predictions: (i) Rural endemic (Portugal mainland) termite populations will exhibit high diversity of symbionts; (ii) invasive urban populations (Horta city, Faial island, Azores), on the contrary, will exhibit lower diversity of symbionts, showing high similarity of symbiont assemblages through environmental filtering; (iii) recent historical colonization of isolated regions—as the case of islands—will imply a loss of symbiont diversity; and (iv) island isolation will trigger a change in colony breeding structure toward a less aggressive behavior. Symbiont flagellate protist communities were morphologically identified, and species richness and relative abundances, as well as biodiversity indices, were used to compare symbiotic communities in colonies from urban and rural environments and between island invasive and mainland endemic populations. To evaluate prediction on the impact of isolation (iv), aggression tests were performed among termites comprising island invasive and mainland endemic populations. A core group of flagellates and secondary facultative symbionts was identified. Termites from rural environments showed, in the majority of observed colonies, more diverse and abundant protist communities, probably confirming prediction (i). Corroborating prediction (ii), the two least diverse communities belong to termites captured inside urban areas. The Azorean invasive termite colonies had more diverse protist communities than expected and prediction (iii) which was not verified within this study. Termites from mainland populations showed a high level of aggressiveness between neighboring colonies, in contrast to the invasive colonies from Horta city, which were not aggressive to neighbors according to prediction (iv). The symbiotic flagellate community of R. grassei showed the ability to change in a way that might be consistent with adaptation to available conditions, possibly contributing to optimization of the colonization of new habitats and spreading of its distribution area, highlighting R. grassei potential as an invasive species.

Understanding the impact of fire on termites in degraded tropical peatlands and the mechanisms for their ecological success: current knowledge and research needs

AbstractPeatlands have experienced large scale changes due to extensive deforestation for logging, conversion to agro‐industrial plantations, and frequent peat fires. The adverse effects of peat fires can lead to long‐term impacts on invertebrate biodiversity in the peatland ecosystem. Although the impact of fire on termite diversity in tropical grasslands and savannas has been the focus of increased attention in recent years, little is known about the effects of peat fires on termite assemblages. In this review, we present available information about the impact of human use of peatlands on termite assemblages in the Indo‐Malayan region. By synthesizing the currently available studies conducted in temperate and tropical savanna systems, we highlight the need for studies of the relationship between termites and fire‐impacted tropical peatlands. We consider the ecological and biological scenarios in fire‐impacted peatland that are likely to shape termite assemblages, and we discuss traits of the surviving genera (i.e., Coptotermes, Schedorhinotermes, and Parrhinotermes) that may contribute to their success in the harsh post‐fire peatland environment (e.g., colony fusion, colony breeding structure, subsidiary nests, and colony migration). Knowledge of these strategies is crucial for understanding the evolutionary adaptation process of termites. This review also aims to stimulate further research in using termite ecosystem services to restore the fertility of degraded fire‐impacted peatlands.

Relationship between invasion success and colony breeding structure in a subterranean termite.

Factors promoting the establishment and colonization success of introduced populations in new environments constitute an important issue in biological invasions. In this context, the respective role of pre-adaptation and evolutionary changes during the invasion process is a key question that requires particular attention. This study compared the colony breeding structure (i.e. number and relatedness among reproductives within colonies) in native and introduced populations of the subterranean pest termite, Reticulitermes flavipes. We generated and analysed a data set of both microsatellite and mtDNA loci on termite samples collected in three introduced populations, one in France and two in Chile, and in the putative source population of French and Chilean infestations that has recently been identified in New Orleans, LA. We also provided a synthesis combining our results with those of previous studies to obtain a global picture of the variation in breeding structure in this species. Whereas most native US populations are mainly composed of colonies headed by monogamous pairs of primary reproductives, all introduced populations exhibit a particular colony breeding structure that is characterized by hundreds of inbreeding reproductives (neotenics) and by a propensity of colonies to fuse, a pattern shared uniquely with the population of New Orleans. These characteristics are comparable to those of many invasive ants and are discussed to play an important role during the invasion process. Our finding that the New Orleans population exhibits the same breeding structure as its related introduced populations suggests that this native population is pre-adapted to invade new ranges.

Characterization of Microsatellites for Population Genetic Analyses of the Fungus-Growing TermiteOdontotermes formosanus(Isoptera: Termitidae)

The fungus-growing subterranean termite Odontotermes formosanus Shiraki (Isoptera: Termitidae) is a destructive pest in Southeast Asia. To facilitate studies on the biology, ecology, and control of O. formosanus, we isolated and characterized nine novel microsatellite loci from a mixed partial genomic library of O. formosanus and the sympatric Macrotermes barneyi Light enriched for di-, tri-, and tetranucleotide repeats. We screened these loci in three populations of O. formosanus from China. All loci were polymorphic. Three loci showed heterozygote deficit possibly because of the presence of null alleles. The remaining six loci with 4-15 alleles per locus and an average observed heterozygosity of 0.15-0.60 across populations were used for population genetic analysis. Populations from different provinces (Guangdong, Jiangxi, and Hubei) were genetically differentiated, but the genetic distance between populations was surprisingly small (FST: 0.03-0.08) and the gene flow was considerable (Nem: 3-8), despite the geographical distance being >300 km. Genetic diversity within populations was low (allelic richness: 5.1-6.3) compared with other subterranean dwelling termites, but consistent with the diversity in species of the family Termitidae. Microsatellite markers developed for O. formosanus will allow further studies to examine the phylogeography, population genetic and colony breeding structure, dispersal ranges, and size of foraging territories in this and closely related species, as well as aid in assessing treatment success.

Clinal variation in colony breeding structure and level of inbreeding in the subterranean termitesReticulitermes flavipesandR. grassei

Social insects exhibit remarkable variation in their colony breeding structures, both within and among species. Ecological factors are believed to be important in shaping reproductive traits of social insect colonies, yet there is little information linking specific environmental variables with differences in breeding structure. Subterranean termites (Rhinotermitidae) show exceptional variation in colony breeding structure, differing in the number of reproductives and degree of inbreeding; colonies can be simple families headed by a single pair of monogamous reproductives (king and queen) or they can be extended families headed by multiple inbreeding neotenic reproductives (wingless individuals). Using microsatellite markers, we characterized colony breeding structure and levels of inbreeding in populations over large parts of the range of the subterranean termites Reticulitermes flavipes in the USA and R. grassei in Europe. Combining these new data with previous results on populations of both species, we found that latitude had a strong effect on the proportion of extended-family colonies in R. flavipes and on levels of inbreeding in both species. We examined the effect of several environmental variables that vary latitudinally; while the degree of inbreeding was greatest in cool, moist habitats in both species, seasonality affected the species differently. Inbreeding in R. flavipes was most strongly associated with climatic variables (mean annual temperature and seasonality), whereas nonclimatic variables, including the availability of wood substrate and soil composition, were important predictors of inbreeding in R. grassei. These results are the first showing that termite breeding structure is shaped by local environmental factors and that species can vary in their responses to these factors.

Genetic diversity and colony breeding structure in native and introduced ranges of the Formosan subterranean termite, Coptotermes formosanus

The Formosan subterranean termite, Coptotermes formosanus is recognized as one of the most important invasive pest species. Originating from China, C. formosanus has spread to many tropical and subtropical regions around the globe in the last 400 years, including Japan, Hawaii and the continental USA. Although the current distribution is well docu- mented, information about the patterns of invasion and effects of introduction on the population genetics of this species is largely lacking. We analyzed the genetic structure of populations from two native populations (Guangdong and Hunan provinces, China) and two introduced populations (Maui and Kauai, Hawaii) using microsatellite genotyping. We also reanalyzed published data of additional populations from China, Japan, Hawaii, and the continental USA. The popula- tion from Hunan, the earliest introduction outside of China (Japan) and the first introduction to the conti- nental USA (South Carolina) showed little genetic similarity with any of the native or introduced popu- lations investigated. However, populations from Oahu (HI), New Orleans (LA) and Rutherford County (NC) showed close similarity. In general, genetic patterns suggest multiple introductions to the USA, with, for example, two separate introductions to the island of Maui. Bottleneck effects were detected in almost all recent introductions (after 1940). All populations in the introduced range showed lower genetic diversity than those in the native range. However, this low genetic diversity did not result in the formation of polygynous supercolonies as has been described for other invasive termite and ant species.

Identification and characterization of 15 polymorphic microsatellite loci in the western drywood termite, Incisitermes minor (Hagen)

Despite recognition of the western drywood termite, Incisitermes minor (Hagen), as one of the most economically important and destructive termite species in the USA, both its population and colony breeding structure genetically remain unclear. Here, we present primer sequences and initial characterization for 15 polymorphic microsatellite loci. In a sample of 30 individuals, representing six geographically distinct locations collected in California, USA, three to 15 alleles were detected segregating per locus. Within a single population observed heterozygosity ranged from 0.050 to 0.866.

Worker Size in the Formosan Subterranean Termite in Relation to Colony Breeding Structure as Inferred from Molecular Markers

The Formosan subterranean termite, Coptotermes formosanus Shiraki, is an invasive species that originated in China and has been introduced to Hawaii and the U.S. mainland. Colonies are headed either by a pair of reproductives (simple families) or by varying numbers of inbreeding reproductives (extended families), and therefore have variable degrees of inbreeding. Worker size also varies among colonies of Formosan termites. We tested whether variation in worker size can be explained by the breeding system. Workers were collected from colonies from three geographically separated populations (China, Hawaii, and Louisiana), and body weight and head size were measured. Microsatellite genotyping was used to establish whether colonies were simple or extended families and to determine the heterozygosity of workers and their degree of inbreeding relative to their colony (FIC, sensitive to the number of reproductives). All Chinese colonies contained multiple inbreeding neotenics. In Hawaii, 37% of the colonies were simple families and 63% were extended families, both having considerable degrees of inbreeding. In Louisiana, 57% of the colonies were simple families, which were mostly headed by unrelated pairs, and 43% were extended families. In simple families, size and body weight of workers were not associated with FIC or heterozygosity. In extended families of two populations, both size parameters were negatively correlated with FIC; however, heterozygosity was not associated with worker size in any of the populations. This suggests that the number of reproductives within colonies has a stronger influence on worker size than the individuals’ genetic diversity in Formosan subterranean termite colonies.

Worker Size in the Formosan Subterranean Termite in Relation to Colony Breeding Structure as Inferred from Molecular Markers

The Formosan subterranean termite, Coptotermes formosanus Shiraki, is an invasive species that originated in China and has been introduced to Hawaii and the U.S. mainland. Colonies are headed either by a pair of reproductives (simple families) or by varying numbers of inbreeding reproductives (extended families), and therefore have variable degrees of inbreeding. Worker size also varies among colonies of Formosan termites. We tested whether variation in worker size can be explained by the breeding system. Workers were collected from colonies from three geographically separated populations (China, Hawaii, and Louisiana), and body weight and head size were measured. Microsatellite genotyping was used to establish whether colonies were simple or extended families and to determine the heterozygosity of workers and their degree of inbreeding relative to their colony (F (IC), sensitive to the number of reproductives). All Chinese colonies contained multiple inbreeding neotenics. In Hawaii, 37% of the colonies were simple families and 63% were extended families, both having considerable degrees of inbreeding. In Louisiana, 57% of the colonies were simple families, which were mostly headed by unrelated pairs, and 43% were extended families. In simple families, size and body weight of workers were not associated with F (IC) or heterozygosity. In extended families of two populations, both size parameters were negatively correlated with F (IC); however, heterozygosity was not associated with worker size in any of the populations. This suggests that the number of reproductives within colonies has a stronger influence on worker size than the individuals' genetic diversity in Formosan subterranean termite colonies.

Comparative Study of Breeding Systems of Sympatric Subterranean Termites (Reticulitermes flavipesandR. hageni) in Central North Carolina Using Two Classes of Molecular Genetic Markers

We used microsatellite and mtDNA markers to compare colony and population genetics of two sympatric species of subterranean termites, Reticulitermes flavipes (Kollar) (n = 25 colonies) and R. hageni Banks (n = 16 colonies), in two sites located 27 km apart in the Piedmont of central North Carolina. Colony breeding structure was inferred by examination of microsatellite genotypes of workers within colonies and by estimates of nestmate relatedness and hierarchical F-statistics. Similar to previous results on this species, nearly one-half of the R. flavipes colonies were simple families mainly headed by outbred primary (alate-derived) reproductives, about one-half were comprised of extended (inbred) families inferred to be headed by low numbers of neotenics (non alate-derived secondary reproductives) descended from the original primary pair, and two colonies contained the offspring of multiple reproductives. About two-thirds of the R. hageni colonies were comprised of simple families largely headed by related reproductives, and about one-third consisted of extended families headed by low numbers of neotenics. R. hageni differed from R. flavipes in having significant isolation by distance at one site as well as significant differentiation between sites at both the microsatellite and mtDNA markers. We conclude that dispersal in R. hageni is more limited resulting in higher levels of inbreeding within colonies and greater degrees of population genetic structure at small and large spatial scales than in sympatric populations of R. flavipes. These results indicate that closely related species of subterranean termites occurring in the same habitat can differ in their breeding systems with important consequences for higher level genetic structure.

Colony Social Organization and Population Genetic Structure of an Introduced Population of Formosan Subterranean Termite from New Orleans, Louisiana

The Formosan subterranean termite, Coptotermes formosanus Shiraki, is an invasive species in many parts of the world, including the U.S. mainland. The reasons for its invasive success may have to do with the flexible social and spatial organization of colonies. We investigated the population and breeding structure of 14 C. formosanus colonies in Louis Armstrong Park, New Orleans, LA. This population has been the focus of extensive study for many years, providing the opportunity to relate aspects of colony breeding structure to previous findings on colony characteristics such as body weight and number of workers, wood consumption, and intercolony aggression. Eight colonies were headed by a single pair of outbred reproductives (simple families), whereas six colonies were headed by low numbers of multiple kings and/or queens that were likely the neotenic descendants of the original colony (extended families). Within the foraging area of one large extended family colony, we found genetic differentiation among different collection sites, suggesting the presence of separate reproductive centers. No significant difference between simple family colonies and extended family colonies was found in worker body weight, soldier body weight, foraging area, population size, or wood consumption. However, level of inbreeding within colonies was negatively correlated with worker body weight and positively correlated with wood consumption. Also, genetic distance between colonies was positively correlated with aggression levels, suggesting a genetic basis to nestmate discrimination cues in this termite population. No obvious trait associated with colony reproductive structure was found that could account for the invasion success of this species.

Genetic analysis of the breeding system of an invasive subterranean termite, Reticulitermes santonensis, in urban and natural habitats

Reticulitermes santonensis is a subterranean termite that invades urban areas in France and elsewhere where it causes damage to human-built structures. We investigated the breeding system, colony and population genetic structure, and mode of dispersal of two French populations of R. santonensis. Termite workers were sampled from 43 and 31 collection points, respectively, from a natural population in west-central France (in and around the island of Oleron) and an urban population (Paris). Ten to 20 workers per collection point were genotyped at nine variable microsatellite loci to determine colony identity and to infer colony breeding structure. There was a total of 26 colonies, some of which were spatially expansive, extending up to 320 linear metres. Altogether, the analysis of genotype distribution, F-statistics and relatedness coefficients suggested that all colonies were extended families headed by numerous neotenics (nonwinged precocious reproductives) probably descended from pairs of primary (winged) reproductives. Isolation by distance among collection points within two large colonies from both populations suggested spatially separated reproductive centres with restricted movement of workers and neotenics. There was a moderate level of genetic differentiation (F(ST) = 0.10) between the Oleron and Paris populations, and the number of alleles was significantly higher in Oleron than in Paris, as expected if the Paris population went through bottlenecks when it was introduced from western France. We hypothesize that the diverse and flexible breeding systems found in subterranean termites pre-adapt them to invade new or marginal habitats. Considering that R. santonensis may be an introduced population of the North American species R. flavipes, a breeding system consisting primarily of extended family colonies containing many neotenic reproductives may facilitate human-mediated spread and establishment of R. santonensis in urban areas with harsh climates.

Microsatellite markers for two species of dampwood termites in the genus Zootermopsis (Isoptera: Termopsidae)

AbstractDampwood termites in the genus Zootermopsis inhabit forested areas in western North America. To better understand the colony composition and breeding structure of Zootermopsis, we identified polymorphic microsatellite loci to use in population analysis. Microsatellite loci were isolated from Zootermopsis nevadensis nevadensis (Hagen); however, all primers amplified homologous loci in Zootermopsis angusticollis (Hagen) and Zootermopsis nevadensis nuttingi (Hagen). Twelve loci were polymorphic in one or more of the above subspecies and species. The number of alleles per locus ranged from one to six, with some allelic differences among subspecies and species. We are currently utilizing the microsatellite markers to investigate the population genetics of Zootermopsis.