Caste differentiation and growth of laboratory colonies of Reticulitermes urbis (Isoptera, Rhinotermitidae)

A total of 280 laboratory colonies of Reticulitermes urbis were raised for 3 years, in order to observe caste differentiation and overall colony growth, and to investigate whether the initial composition (0, 2 or 4 nymphs; 0, 5, 10, 20 or 50 workers) affected colony survival, population growth and other colony dynamics. We also wanted to determine the minimum number of individuals needed to establish a vital colony. As a result, every colony beginning with less than 20 workers died within 60 weeks, while colonies beginning with at least 20 workers survived until the end of the tests, with varied survival rates dependent upon the initial size and the time of formation (summer or autumn). The number of nymphs did not affect colony survival and colony growth. Reproductives developed from nymphs within 2 weeks and later from workers. Many of the reproductives derived from nymphs were killed by workers. The majority of the colonies contained two reproductives 3 years after initiating the tests. In addition, a few individual workers were still alive at the end of the 3-year tests. At the end of the tests, the proportion of soldiers ranged anywhere from 5.23 to 7.69% of the total population. The number of viable “juveniles” from each colony was relatively low throughout the tests and the overall population growth was not sufficient enough to replace dead workers or increase the colony size considerably. These results indicate that the potential to establish viable and sustainable colonies for groups of R. urbis composed of 5–50 workers is very low.     

Asexual queen succession mediates an accelerated colony life cycle in the termite Silvestritermes minutus

Mixed modes of reproduction, combining sexual processes with thelytokous parthenogenesis, occur in all major clades of social insects. In several species of termites, queens maximize their genetic input into nondispersing replacement queens through parthenogenesis, while maintaining genetically diverse sterile offspring and dispersing reproductives via sexual reproduction. This so‐called asexual queen succession (AQS) has multiple independent origins and its presumed advantages are diverse as well, ranging from multiplication of colony reproductive potential to extension of its lifespan beyond that of the foundress. However, how AQS shapes colony life cycles under natural conditions remains poorly known. The neotropical termite Silvestritermes minutus inhabits small but conspicuous nests, offering a unique opportunity to investigate the impact of AQS on life history. We report on its breeding system, life cycle and sex allocation using social structure census in 137 nests and genotyping of 12 colonies at 12 microsatellite loci. We show that colonies are established by an outbred pair of primary reproductives. In less than 2 years, the foundress is replaced by multiple neotenic queens, arising mostly through automixis with central fusion. Sterile castes, male and most (93%) female dispersers are produced sexually. Colony reproduction is usually restricted to a single dispersal of alates with unbiased sex ratio, taking place after 3 years. We conclude that S. minutus benefits from AQS to maximize colony growth rate and alate production within a very short life cycle rather than to extend colony lifespan. This highlights the versatile role of AQS in different cases of its polyphyletic origin.     

Clinal variation in colony breeding structure and level of inbreeding in the subterranean termites Reticulitermes flavipes and R. 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.     

Geographical distribution,genetic diversity and social organization of a new European termite, <Emphasis Type="Italic">Reticulitermes urbis</Emphasis> (Isoptera: Rhinotermitidae)

Reticulitermes urbis is a recently described termite species that has probably been introduced into Western Europe where it has been found exclusively in urban areas. However, little is known about the geographic distribution and origin of R. urbis. This study was undertaken to determine whether this species was introduced from the Balkans. A parsimony network did not show any association between mtDNA haplotypes and geographic regions suggesting that western European populations were the result of human-mediated dispersion. Variation patterns of the COI and COII regions as well as microsatellites showed that the genetic diversity of Western European colonies was lower than for colonies collected in the Balkans, suggesting that the introduced populations suffered from a founder effect. As observed in the introduced populations of R. flavipes, all colonies of R. urbis had an extended-family structure with several reproductives. These results support the scenario that this termite was introduced into Western Europe.     

Asexual queen succession in the higher termite Embiratermes neotenicus

Asexual queen succession (AQS), in which workers, soldiers and dispersing reproductives are produced sexually while numerous non-dispersing queens arise through thelytokous parthenogenesis, has recently been described in three species of lower termites of the genus Reticulitermes. Here, we show that AQS is not an oddity restricted to a single genus of lower termites, but a more widespread strategy occurring also in the most advanced termite group, the higher termites (Termitidae). We analysed the genetic structure in 10 colonies of the Neotropical higher termite Embiratermes neotenicus (Syntermitinae) using five newly developed polymorphic microsatellite loci. The colonies contained one primary king accompanied either by a single primary queen or by up to almost 200 neotenic queens. While the workers, the soldiers and most future dispersing reproductives were produced sexually, the non-dispersing neotenic queens originated through thelytokous parthenogenesis of the founding primary queen. Surprisingly, the mode of thelytoky observed in E. neotenicus is most probably automixis with central fusion, contrasting with the automixis with terminal fusion documented in Reticulitermes. The occurrence of AQS based on different mechanisms of ploidy restoration raises the hypothesis of an independent evolutionary origin of this unique reproductive strategy in individual lineages of lower and higher termites.     

The Non-LTR Retrotransposon R2 in Termites (Insecta,Isoptera): Characterization and Dynamics

The full-length element of the non-LTR retrotransposon R2 is here characterized in three European isopteran species: the more primitive Kalotermes flavicollis (Kalotermitidae), including two highly divergent mitochondrial lineages, and the more derived Reticulitermes lucifugus and R. urbis (Rhinotermitidae). Partial 3′ sequences for R. grassei and R. balkanensis were also analyzed. The essential structural features of R2 elements are conserved in termites. Phylogenetic analysis revealed that termite elements belong to the same clade and that their phylogeny is fully compatible with the phylogeny of their host species. The study of the number and the frequency of R2 insertion variants in four R. urbis colonies suggests a greatly reduced, or completely absent, recent element activity.     

Does lack of intraspecific aggression or absence of nymphs determine acceptance of foreign reproductives in <Emphasis Type="Italic">Macrotermes</Emphasis>?

The rejection or acceptance of a foreign reproductive by an alien colony may not always be as straightforward as cue recognition between worker termites. This paper aims to determine whether adoption of foreign reproductives is caused simply by lack of intraspecific aggression or is contingent on the reproductive status of the host colony. In the fungus-culturing termites, Macrotermes gilvus (Hagen) and Macrotermes carbonarius (Hagen), major workers showed low intraspecific aggression towards non-nestmates irrespective of geographic distance between source colonies. Our results indicated that workers were hardly aggressive towards non-nestmates. In royal cell-swapping experiments, both species responded in a similar way: (1) in host colonies with nymphs present, the foreign reproductives were rejected; while (2) in host colonies without nymphs the foreign reproductives were either accepted and breeding resumed or the host colonies died eventually. Workers from the host colonies preferentially maintained offspring nymphs from which adultoid replacement reproductives develop rather than accepting foreign reproductives. There is no fitness gain for the queenless workers in accepting foreign reproductives; however, there is overall benefit to the newly born population.     

Extreme genetic mixing within colonies of the wood-dwelling termite Kalotermes flavicollis (Isoptera,Kalotermitidae)

The existence of altruism in social insects is commonly attributed to altruistic individuals gaining indirect fitness through kin selection. However, recent studies suggest that such individuals might also gain direct fitness through reproduction. Experimental studies on primitive wood-dwelling termites revealed that colony fusion often causes the death of primary reproductives (queen and king), allowing opportunities for workers to inherit the nest by developing into replacement reproductives (neotenics). Therefore, colony fusion has been proposed as an important factor that may have favoured sociality in termites. However, whether colony fusion occurs frequently in natural populations of wood-dwelling termites remains an open question. We analysed eleven colonies of the wood-dwelling termite Kalotermes flavicollis (Kalotermitidae), using two mitochondrial and five nuclear microsatellite markers. Nine of eleven colonies (82%) were mixed families, with offspring of three or more primary reproductives. To our knowledge, this result represents the highest frequency of mixed-family colonies ever reported in termites. Moreover, genetic mixing of colonies appeared extreme in two ways. First, the number of haplotypes per colony was exceptionally high (up to nine), indicating that colonies were composed of multiple queens' offspring. Second, some mixed-family colonies included individuals belonging to two highly divergent genetic lineages. F-statistics and relatedness values suggest that mixed-family colonies most likely result from colony fusion, giving support to the accelerated nest inheritance theory. These findings raise important questions about the mode of foundation of mixed-family colonies and the evolutionary forces that maintain them within populations.     

Developmental plasticity in the queen-polymorphic ant Temnothorax longispinosus

Females of social Hymenoptera show developmental plasticity in response to varying social and environmental conditions, though some species have strong genetic influences on the form of the female reproductives. In ants, a queen polymorphism can occur in which large queens initiate new colonies on their own, while small queens enter established nests. Most queen polymorphisms studied to date originate due to genetic differences between individuals of differing form. Here, we report on the development of female form in response to social factors within the nest in the queen-polymorphic ant Temnothorax longispinosus. Three queen size morphs occur: a rare large queen with higher fat stores that can found new colonies independently, a large queen that has low fat stores and is behaviorally flexible, and a small queen that rejoins the natal nest. Both in nesting units collected from the field and those reared in the lab, queen presence during larval development led to fewer larvae developing as gynes (virgin, winged queens), and most of those gynes were the small morph. This queen effect is transferred to developing gyne larvae by close, physical interaction between queens and workers, and causes slower larval development. We conclude that gyne size, and therefore reproductive behavior, in T. longispinosus is developmentally plastic in response to queen presence. Plasticity in reproductive behavior may be an adaptive response to the nest sites utilized by this species. T. longispinosus nests predominantly in acorns and hickory nuts, which can vary dramatically from 1 year to the next. Since queens are more likely to be present in each nesting unit when fewer nest sites are available, the queen effect that results in more small gynes produced links the expression of colony-founding traits to ecological conditions across habitat patches.     

Population structure and colony composition of two Zootermopsis nevadensis subspecies

Understanding the origin and maintenance of eusociality in termites has proved problematic, in part, due to a lack of knowledge concerning the variability and evolutionary changes in termite breeding structure. One way to address this is to compare the population genetics of a broad range of termite species. However, few studies have investigated the population genetics of basal termite taxa. We used 12 polymorphic microsatellite loci to characterize and compare the colony genetic structure of 18 colonies of two basal termite subspecies, Zootermopsis nevadensis nevadensis and Zootermopsis nevadensis nuttingi. The average relatedness (r) among individuals within a colony was high (0.59) and similar to values reported for other termite species. Average relatedness between colony founders was lower (0.21) suggesting the alates outbreed. Genotypes of workers and soldiers in 4 out of the 18 colonies were consistent with reproduction by a single pair of primary reproductives and the remaining colonies were inferred to have been derived from more than two reproductives. Eleven colonies with three or more reproductives were consistent with replacement reproductives (neotenics) and the remaining three colonies included genetic contribution from three or more primary reproductives. Comparisons between the subspecies revealed significant differences in breeding structure, specifically in the number and types of reproductives (that is, primaries or neotenics). Furthermore, we observed a larger proportion of colonies with greater than three primary reproductives compared to more derived termite lineages. Thus, our results suggest that breeding structure can vary significantly among termite taxa.     

Alate susceptibility in ants

Pathogens are predicted to pose a particular threat to eusocial insects because infections can spread rapidly in colonies with high densities of closely related individuals. In ants, there are two major castes: workers and reproductives. Sterile workers receive no direct benefit from investing in immunity, but can gain indirect fitness benefits if their immunity aids the survival of their fertile siblings. Virgin reproductives (alates), on the other hand, may be able to increase their investment in reproduction, rather than in immunity, because of the protection they receive from workers. Thus, we expect colonies to have highly immune workers, but relatively more susceptible alates. We examined the survival of workers, gynes, and males of nine ant species collected in Peru and Canada when exposed to the entomopathogenic fungus Beauveria bassiana. For the seven species in which treatment with B. bassiana increased ant mortality relative to controls, we found workers were significantly less susceptible compared with both alate sexes. Female and male alates did not differ significantly in their immunocompetence. Our results suggest that, as with other nonreproductive tasks in ant colonies like foraging and nest maintenance, workers have primary responsibility for colony immunity, allowing alates to specialize on reproduction. We highlight the importance of colony‐level selection on individual immunity in ants and other eusocial organisms.     

High occurrence of colony fusion in a European population of the American termite Reticulitermes flavipes

The coexistence of multiple unrelated reproductives within social insect colonies decreases the relatedness among colony members and therefore challenges kin selection theory. This study investigated the colony genetic structure of a French introduced population of the American subterranean termite Reticulitermes flavipes by analyzing genotypes at eight microsatellite loci and at one mtDNA region. Results revealed that all colonies contained numerous related secondary reproductives, and that 31% of colonies possessed more than two unrelated reproductives. The presence of several unrelated reproductives within colonies of this species is commonly assumed to result from colony fusion. Although such a high occurrence of colony fusion is the highest ever observed in a termite population, it is probable that the available methodology underestimated the detection of colony fusion in French populations. Overall, these results suggest that French colonies might differ strongly from the great majority of American colonies in their capacity to produce secondary reproductives as well as in their ability to merge. The nature and evolutionary origin of these population differences are discussed.     

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.     

Colony genetic organization and colony fusion in the termite Reticulitermes flavipes as revealed by foraging patterns over time and space

Temporal and spatial analyses are seldom utilized in the study of colony genetic structure, but they are potentially powerful methods which can yield novel insights into the mechanisms underlying variation in breeding systems. Here we present the results of a study which incorporated both of these dimensions in an examination of genetic structure of subterranean termites in the genus Reticulitermes (primarily R. flavipes). Most colonies of this species (70%) were simple families apparently headed by outbred primary reproductives, while most of the remaining (27% of the total) colonies contained low effective numbers of moderately inbred reproductives. Mapping the spatial distribution of colony foraging sites over time revealed that despite the high colony density, the absolute foraging boundaries of most R. flavipes colonies were persistent and exclusive of other conspecific colonies, which suggests that this species is more territorial than has been implied by laboratory studies of intraspecific aggression. Nevertheless, we found a single colony (3% of all colonies) which contained the offspring of more than two unrelated reproductives. Although other studies have also described subterranean termite colonies with a similarly complex genetic composition, we demonstrate here that such colonies can form under natural conditions via the fusion of whole colonies. This study underscores how repeated sampling from individual colonies over time and space can yield information about colony spatial and genetic structure that cannot be obtained from conventional analyses or sampling methods.     

Comparative study of incipient colony development in the Formosan subterranean termite, <Emphasis Type="Italic">Coptotermes formosanus</Emphasis> Shiraki (Isoptera,Rhinotermitidae)

Summary The Formosan subterranean termite, Coptotermes formosanus Shiraki is the most destructive, difficult to control and economically important species of termite in the southern United States. At present, no information is available on the genetic relatedness of primary Formosan subterranean termite reproductives that establish new colonies. Information on survivorship and fitness components of primary reproductives from different sibships (sibling or nonsibling) is helpful to our understanding of biological and ecological characteristics of different breeding generations in C. formosanus. The present study examined the effects of sibship and colony origin on growth and mortality of incipient colonies of C. formosanus. Seven stock colonies of C. formosanus were collected in 1996 through 1997 in New Orleans and Lake Charles, La, USA. A total of 338 incipient colonies of sibling pairs or nonsibling pairs of C. formosanus were set up. The study indicated that mate relatedness significantly affected mortality and fitness. Nonsibling mates suffered significantly higher mortality than sibling mates originated from New Orleans. However, the decreased success of outbred mates was offset by an increased fecundity compared to inbred colonies over time. Both sibling- and nonsibling-founded colonies from Lake Charles had a significantly higher survival rate than did colonies from New Orleans. Colonies from Lake Charles also produced a significantly higher number of larvae/workers than colonies from New Orleans. The mismatch of habits by mates from different locations and the potential for greater disease risks may be associated with higher mortality in outbred pairs. However, heterozygous offspring of outbred pairs probably have increased genetic variation, which provides greater adaptation potential, thus making the colony more robust in the face of environmental fluctuations.Received 11 March 2002; revised 26 February 2003; accepted 14 March 2003.     

Permanent loss of wings in queens of the ant <Emphasis Type="Italic">Odontomachus coquereli</Emphasis> from Madagascar

Winged queens are the most common reproductives in ants. They are morphologically specialized for independent colony foundation, with wings for long-range dispersal and metabolic reserves to raise the first brood. However independent foundation can sometimes be selected against and replaced by fission, featuring short-range dispersal on the ground and reproductives that are dependent on the wingless workers for all non-reproductive tasks. We investigated the evolutionary consequences of this transition on the morphology of the reproductives by collecting 30 colonies of Odontomachus coquereli from Madagascar, the only species in the genus where winged queens have never been found. Data about colony demography, morphometry, allometry and ovarian dissections showed that the winged queen caste has been replaced by a wingless reproductive caste with distinct body proportions relative to the workers or to congeneric winged queens. The 17 reproductives that we measured exhibited little size variability. A single wingless reproductive was found in each colony, corresponding to ‘ergatoids’ in literature. Several facts suggest that colonies reproduce by fission, notably the relatively constant colony size (19±11 workers). The developmental origins of wingless reproductive phenotypes need investigation; little genetic change may be involved, as seen when Odontomachus larvae are parasitized by nematodes. The sole function of wingless reproductives in O. coquereli is reproduction, and they contrast with multi-purpose wingless reproductives found in other ants, where numerous intermorphs occur in each colony and contribute to sterile tasks. Received 15 December 2006; revised 26 February 2007; accepted 1 March 2007.     

Optional gamergates in the queenright ponerine ant Gnamptogenys striatula Mayr

Summary: Ponerine ants display a number of social structures to which particular behaviours are associated. In the ponerine ant species Gnamptogenys striatula Mayr, queens occur and queenright colonies are functionally polygynous. However, some workers are capable to mate and to produce their own worker offspring. These gamergates appear several days after the queens are experimentally removed, allowing some workers to adopt a sexual calling posture inside the nest. At that time, other workers get outside the nest to collect males in the arena and carry them back into the colony. There, these males are groomed before they can mate with sexual calling workers. As for queens, several gamergates may coexist in a same colony. The social profile of gamergates is similar to those of nurses and they stay closer to the egg piles.     

An American termite in Paris: temporal colony dynamics

Termites of the genus Reticulitermes are widespread invaders, particularly in urban habitats. Their cryptic and subterranean lifestyle makes them difficult to detect, and we know little about their colony dynamics over time. In this study we examined the persistence of Reticulitermes flavipes (Kollar) colonies in the city of Paris over a period of 15 years. The aim was (1) to define the boundaries of colonies sampled within the same four areas over two sampling periods, (2) to determine whether the colonies identified during the first sampling period persisted to the second sampling period, and (3) to compare the results obtained when colonies were delineated using a standard population genetic approach versus a Bayesian clustering method that combined both spatial and genetic information. Herein, colony delineations were inferred from genetic differences at nine microsatellite loci and one mitochondrial locus. Four of the 18 identified colonies did not show significant differences in their genotype distributions between the two sampling periods. While allelic richness was low, making it hard to reliably distinguish colony family type, most colonies appeared to retain the same breeding structure over time. These large and expansive colonies showed an important ability to fuse (39% were mixed-family colonies), contained hundreds of reproductives and displayed evidence of isolation-by-distance, suggesting budding dispersal. These traits, which favor colony persistence over time, present a challenge for pest control efforts, which apply treatment locally. The other colonies showed significant differences, but we cannot exclude the possibility that their genotype distributions simply changed over time.     

Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites

Abstract.

• 1 In natural populations, colonies of bumble bees vary in many important life history traits, such as colony size and age at maturity, or the number and sex of reproductives produced. We investigated how the presence of parasites in field populations of the bumble bee Bombus lucorum L. relates to variation in life history traits and reproductive performance. A total of thirty-six colonies was placed in accessible nest sites in the field and monitored at regular intervals throughout a season.
• 2 Among the life history correlates, early nest foundation was strongly associated with large maximum colony size, old age and large size at maturity, and this in turn with successful production of males and queens, as well as with the number of sexuals produced. Overall, reproductive success was highly skewed with only five colonies producing all the queens. Sixteen colonies failed to reproduce altogether.
• 3 The social parasite Psithyrus was abundant early in the Bombus colony cycle and preferentially invaded host nests with many first brood workers and thus disproportionately large size, i.e. those colonies that would otherwise be more likely to reproduce or produce (daughter) queens rather than males. To prevent nest loss, Psithyrus had to be removed soon after invasion. Therefore, the effects reported here can only be crude estimates.
• 4 Parasitoid conopid flies are likely to cause heavy worker mortality when sexuals are reared by the colonies. Their inferred effect was a reduction in biomass that could be invested in sexuals as well as a shift in the sex ratio at the population level resulting from failure to produce queens. We suggest to group the inferred correlates into ‘early events’ surrounding colony initiation and social parasitism, and ‘late events’ surrounding attained colony size in summer and parasitism by conopid flies. Our evidence thus provides a heuristic approach to understand the factors that affect reproductive success of Bombus colonies.

     

Reproductives and eggs trigger worker vibration in a subterranean termite

In insect societies, the presence of reproductives or eggs has been shown to shape several biological traits in the colony members. Social interactions are one of these traits that involve modification of the communication system of the entire colony. Many studies described the role of chemical compounds and dominance behaviors in the presence of reproductive but vibratory behaviors received very few investigations. Yet, vibratory behaviors are ideal candidates, particularly for subterranean species like termites, as they could be quickly transmitted through the substrate and could be very diversified (origin, modulation). Here, we investigated whether the presence of reproductives/eggs affects the vibratory behavior (body‐shaking) of workers in the subterranean termite Reticulitermes flavipes. Our results reveal that the presence of reproductives or eggs triggers an increase of workers' body‐shaking, independent of their colony of origin after 24 hr. We hypothesize that vibratory communication could be used to transfer information about the presence of reproductives and eggs to the entire colony, suggesting that vibratory behaviors could serve as an important yet neglected mediator of social regulation.