Density triggers soldier production in a social aphid

For evolution and maintenance of the social system of insect colonies, investment in the sterile caste should be adequately controlled in response to environmental cues. Recent developments using artificial diet rearing techniques have revealed an underlying mechanism of caste control in a gall-forming aphid, Tuberaphis styraci, which has a soldier caste in the second instar. Statistical analyses of field-collected galls detected a significant positive correlation between aphid density and soldier proportion in the natural colonies of T. styraci. Artificial diet experiments showed that soldiers are produced under crowded conditions. Detailed experiments demonstrated that soldiers are produced in a density-dependent manner rather than in a colony size-dependent manner. From these results, it was concluded that aphid density is the crucial cue that triggers soldier production in T. styraci. This study provides, to our knowledge, the first experimental demonstration of an environmental factor involved in aphid soldier differentiation.     

The proximate cue of density-dependent soldier production in a social aphid

Tuberaphis styraci is a social aphid that produces 2nd instar soldiers with morphological, behavioral and reproductive division. High aphid density was shown to induce soldier production in T. styraci, although direct cue of soldier induction associated with high density has been unknown. In order to identify the proximate environmental cue underlying the density-dependent soldier production, a series of experiments was conducted using an artificial diet rearing technique. When adult aphids were reared with live normal nymphs, live soldiers, dead normal nymphs, shed skins, honeydew globules and excreted wax, only live normal nymphs effectively induced soldier production. In order to gain insights into the nature of soldier-inducing cue associated with normal aphids, we performed artificial diet experiments using partitioned and non-partitioned chambers, in which direct contact between aphids was either inhibited or allowed. Induction of soldiers was observed only when direct contact was allowed. Therefore, it was shown that the soldier-inducing cue is neither volatile in the air nor diffusible through the diet, but is transmitted between normal non-soldier aphids via direct contact. On the basis of these results, we suggest that the soldier-inducing cue might be physical stimulus combined with non-volatile surface chemicals whose properties differ between normal aphids and soldiers.     

Density-dependent induction and suppression of soldier differentiation in an aphid social system

We investigated the mechanism underlying the control of soldier production in colonies of a social aphid, Tuberaphis styraci, which has a sterile soldier caste in the second instar. High aphid density was shown to induce soldier production in T. styraci. Analysis of natural colonies revealed that the soldier proportion tended to increase with aphid density but reached a plateau. Artificial diet experiments identified a similar plateau of soldier proportion under high-density conditions. In order to gain insights into the controlling mechanism of soldier production, the effect of soldiers on reproducing adult aphids was examined using the artificial diet system. It was experimentally demonstrated that soldier production was suppressed by coexisting soldiers, whereas coexisting non-soldiers facilitated soldier production. These results suggested that caste ratio in the colony of T. styraci is controlled by positive and negative feedbacks consisting of density-dependent induction and suppression of soldier differentiation.     

Alate production in an aphid in relation to ant tending and alarm pheromone

1. Winged dispersal is vital for aphids as predation pressure and host plant conditions fluctuate. 2. Ant‐tended aphids also need to disperse, but this may represent a cost for the ants, resulting in an evolutionary conflict of interest over aphid dispersal. 3. The combined effects of aphid alarm pheromone, indicating predation risk, and ant attendance on the production of winged aphids were examined in an experiment with Aphis fabae (Homoptera: Aphididae) (Scopoli 1763) aphids and Lasius niger (Formicidae: Formicinae) (Linné, 1758) ants. 4. This study is the first to investigate the joint effects of alarm pheromone and ant attendance, and also the first to detect an influence of alarm pheromone on the production of winged morphs in A. fabae. 5. After a period of 2 weeks, it was found that aphid colonies exposed to intermittent doses of alarm pheromone produced more winged individuals, whereas ant tending had the opposite effect. The effects were additive on a log scale, and ant attendance had a greater proportional influence than exposure to alarm pheromone. A tentative conclusion is that ants have gained the upper hand in an evolutionary conflict about aphid dispersal.     

Seasonal extension of the soldier instar as a route to increased defence investment in the social aphid Pemphigus spyrothecae

Abstract.  1. The possibility that the duration of the soldier instar could be extended over the course of the galling season was examined in Pemphigus spyrothecae Passerini (Hemiptera: Aphididae). In this species, the individuals of one morph of the dimorphic first instar are non-sterile specialised defenders known as soldiers.
2. In the face of a declining birth rate, the proportion of first-instar soldiers to first-instar non-soldiers was found to increase. This provides strong evidence of extension of the soldier instar over time.
3. Instar extension provides a mechanism for post-natal investment in soldiers and allows individuals with insufficient time to mature to remain in the defensive stage so that they may continue to make an indirect contribution to their clone's reproductive success.     

黑蚁对雪松长足大蚜集群时空变化的取食反应

我们研究了黑蚁 (Lasiusniger)如何开发距离其巢不同距离的多种食物资源 ,以及黑蚁的照看活动是否与雪松长足大蚜 (Cinaracedri)种群的增长有关 ,以及 /或者受空间分布的影响。笔者定期调查了Cinaracedri集群的空间分布 ,以及在雪松树枝上黑蚁取食的时间变化 ,发现只有 2 5 %的蚜虫集群在研究后数周内保持在同样的位置 ,这表明蚜虫集群的高度运动性迫使黑蚁改变活动路线以获取事物资源。实际上 ,黑蚁集群能选择最近的食物资源以及蚜虫数量最多的地点     

Ant semiochemicals limit apterous aphid dispersal

Some organisms can manipulate the nervous systems of others or alter their physiology in order to obtain benefit. Ants are known to limit alate aphid dispersal by physically removing wings and also through chemical manipulation of the alate developmental pathway. This results in reduced dispersal and higher local densities of aphids, which benefit ants in terms of increased honeydew and prey availability. Here, we show that the walking movement of mutualistic apterous aphids is also reduced by ant semiochemicals. Aphids walk slower and their dispersal from an unsuitable patch is hampered by ants. If aphid walking dispersal has evolved as a means of natural enemy escape, then ant chemicals may act as a signal indicating protection; hence, reduced dispersal could be adaptive for aphids. If, however, dispersal is primarily a means to reduce competition or to maintain persistent metapopulations, then manipulation by ants could be detrimental. Such manipulation strategies, common in host-parasite and predator-prey interactions, may be more common in mutualism than expected.     

Female production within the gall and male production on leaves by individual alates of a social aphid

The social aphid Astegopteryx spinocephala forms a banana-bunch shaped gall, consisting of several subgalls, on Styrax benzoides in northern Thailand. The aphid’s life cycle is non-host alternating. Alates (sexuparae) containing both male and female embryos appear near the end of the dry season, when many sexuals and eggs are found in subgalls guarded by sterile soldiers. Our experiments revealed that these alates give birth to almost all (99%) females within the natal subgall before flying but most (73–86%) males on leaves of the host tree after flying, and that these first-instar males intrude into live subgalls for mating. The fact that some (14–27%) males are deposited in the natal subgall indicates the occurrence of both outbreeding and inbreeding, or some level of local mate competition (LMC), in this mating system. However, the primary (investment) sex ratio was estimated to be near 0.5. This suggests that factors other than LMC, a candidate for which is local resource competition, might also affect the sex ratio in A. spinocephala. Received 19 March 2007; revised 12 July 2007; accepted 13 August 2007.     

Dietary influences on aphid polymorphism

Polymorphism in aphids is the general rule. The occurrence and succession of their different morphs in nature has been related to numerous factors. Whereas some of these factors may already influence the morph of the generation exposed to them, others express themselves only in subsequent generations. Major, and sometimes exclusive, importance has been attached to environmental temperature and daylength acting directly on the aphids to induce the production of sexual morphs, and to interactions between aphids in the development of winged individuals or in the production of alate progeny.Although various physiological conditions of the hostplants of aphids have for decades been implicated in the development of winged populations, unequivocal evidence that hostplants do play a role in morph determination has not until recently been obtained. Evidence that dietary factors are indeed involved is currently being obtained by using chemically defined artificial diets.Although non-dietary factors may largely determine which of several genetically possible morphs predominantly express themselves, it is now quite clear from the studies to be reported that dietary factors can have a modifying and sometimes even a dominant effect on the processes affecting the morphological expression of aphids.

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Zusammenfassung Polymorphismus ist bei den Aphiden die Regel. Das Auftreten und die Aufeinanderfolge ihrer verschiedenen Morphen in der Natur ist auf zahlreiche Faktoren bezogen worden. Während einige dieser Faktoren bereits die Morphen der Generation zu beeinflussen vermögen, die ihnen ausgesetzt ist, kommen andere erst in den folgenden Generationen zum Ausdruck. Überwiegende und manchmal ausschließliche Bedeutung wurde der Umgebungstemperatur und der Tageslänge zugemessen, die direkt auf die Induktion der Erzeugung von Sexualformen wirken, sowie den Wechselwirkungen zwischen Blattläusen bei der Entwicklung geflügelter Individuen oder bei der Produktion einer geflügelten Nachkommenschaft.Obwohl verschiedene physiologische Zustände der Wirtspflanzen der Blattläuse seit Jahrzehnten mit der Entwicklung geflügelter Populationen in Zusammenhang gebracht worden sind, wurde ein unumstößlicher Nachweis, daß Wirtspflanzen tatsächlich eine Rolle bei der Morphendetermination spielen, bis vor kurzem nicht erbracht. Nachweise, daß Nahrungsfaktoren tatsächlich mitspielen, wurden fortlaufend bei der Benutzung chemisch definierter künstlicher Diäten erhalten.Obwohl Nicht-Nahrungsfaktoren weitgehend bestimmen können, welche der verschiedenen genetisch möglichen Morphen vorwiegend zur Verwirklichung kommen, so geht doch aus den hier vorliegenden Untersuchungen nunmehr völlig klar hervor, daß Nahrungsfaktoren eine modifizierende, manchmal sogar eine beherrschende Wirkung auf die Prozesse ausüben können, welche die morphologische Ausbildung der Blattläuse beeinflussen.

     

Reproductive schedule and factors affecting soldier production in the eusocial bamboo aphid Pseudoregma bambucicola (Homoptera, Aphididae)

Summary: The reproductive characteristics of the soldier-producing aphid Pseudoregma bambucicola were studied in Kagoshima, Southern Japan, to know the factors affecting soldier production of eusocial aphids. The soldier proportion in aphid colonies was highest from October to November. In some large colonies, soldiers were observed in all seasons except in July when colony size was relatively small. Multiple regression analysis showed that the colony size was a principal factor affecting soldier proportion throughout a year. Other social or environmental factors such as aphid composition, host plant conditions and predator abundance were not always significant. Rearing experiments revealed that large colonies (̿,000 individuals) produced soldiers in almost all seasons while small colonies (<1,000) never produced any soldiers. The caste-production schedule of adult females was examined in the field. When solitary females produced both castes, they usually produced normal nymphs first and then soldiers. Females from large colonies tended to produce more soldiers in the earlier period of their lifetime, whereas females from newly established small colonies produced no or only a few soldiers at later times. The average number of soldiers and normal nymphs produced consecutively by a single female was >10 and >20, respectively. Because they have a small number of ovarioles (<15 on average), females should alter caste production within the same ovarioles according to changes in environmental conditions. Artificial removal or introduction of predators and reduction of colony size did not affect soldier production over two successive generations, revealing maternal effects on soldier production. Females cannot shift caste production quickly in response to changes in predator abundance and colony size. This is probably due to early developmental determination of castes within the mother's body.     

The evolution of soldier reproduction in social thrips

We estimated the degree of reproductive differentiation betweenfoundresses and soldiers in multiple populations of five speciesof haplodiploid Australian gall-forming thrips using microsatellitedata, ovarian dissections, and census data. Microsatellite-basedspecies estimates of average per capita reproductive outputof soldiers relative to the foundresses ranged from 0.005 to0.64, and dissection and census-based estimates ranged from0.17 to 1.1. Mapping of these estimates onto a phylogeny showedthat levels of soldier reproduction were apparently higherin three basal lineages than in two more derived lineages.We infer from this phylogenetic pattern that soldier morphologyand behavior of thrips evolved in the presence of substantial levels of soldier reproduction. This pattern of evolutionarychange is similar to that proposed for the origin of soldiersin aphids and termites, but it differs from the scenario proposedfor the origin of workers in Hymenoptera, within which helpingand strong reproductive division of labor apparently evolvedbefore morphological differentiation. We suggest that this difference in evolutionary routes to eusociality between taxa with soldiersand taxa with foraging workers was driven by a weaker trade-offbetween helping and reproducing, and a greater ability of thehelpers to withstand reproductive domination, in taxa withsoldiers. This is the first study to analyze the social-evolutionarytrajectories of reproductive, behavioral, and morphologicaldifferentiation in the context of a species-level phylogeny.     

Logistic model for soldier production in aphids

Summary The number of aphid soldiers in a colony is positively correlated with colony size. This positive correlation has been repeatedly confirmed for the bamboo aphid Pseudoregma bambucicola. To explain this, we present a simple model assuming logistic growth of the aphid colony. The model predicts that a first soldier is more readily produced in large colonies than in small colonies. This is because the productivity of each reproductive decreases as the colony size increases, and also because the efficiency of defense increases as the number of reproductives defended by the soldier increases. The latter effect disappears when the number of reproductives exceeds N_p, the critical number of reproductives that a predator could damage. This argument holds for a second, a third, and an ith soldier in general. Although we assume logistic growth of the aphid colony, the model is applicable to any form of colony growth with minor changes of some premises.Received 12 February 2003; revised 28 March 2003; accepted 22 April 2003.     

Context‐dependence in an ant–aphid mutualism: direct effects of tending intensity on aphid performance

1. In ant–hemipteran mutualisms, ants receive carbohydrates in the form of honeydew, while hemipterans receive protection from natural enemies. In the absence of natural enemies, however, the direct effects of tending are generally less well known. We hypothesised that with increasing tending intensity (ant to aphid ratio), aphid performance would increase initially, then decrease at high tending levels due to the metabolic cost of producing high quality honeydew. 2. We tested our hypothesis in a greenhouse experiment by manipulating Argentine ant (Linepithema humile Mayr) colony size while holding constant the initial size of aphid (Chaitophorus populicola Thomas) aggregations. The two parameters associated with survival, aphid survivorship to maturity and longevity, declined with increasing tending intensity, whereas per capita birth rate and time to first reproduction showed no relationship to attendance. The intrinsic rate of increase declined only at relatively high tending levels, suggesting a nonlinearity in the effect of tending intensity. 3. Tending intensity measured in the experiment was similar to that observed in free‐living aggregations of C. populicola. Furthermore, the per capita recruitment rate of ants to free‐living aphid aggregations was negatively density‐dependent, indicating that small aggregations tend to experience the highest levels of tending intensity. This finding suggests that the aphid's intrinsic rate of increase may be positively density‐dependent, mediated by the aphid's mutualistic interaction with the ant. 4. In the Argentine ant–C. populicola interaction, experimental manipulation of colony size revealed a direct cost of ant attendance that was conditional upon tending intensity. Experiments that manipulate only ant presence or absence may yield an incomplete understanding of the mutualistic interaction if underlying nonlinearities exist.     

The response of an aphid tending ant to artificial extra-floral nectaries on different host plants

Sap-feeding homopterans, which reduce the fitness of their host plants, are often tended by ants that feed on their honeydew. The composition of the honeydew varies with both the aphid and the host plant. Extra-floral nectaries (EFNs) are believed to have evolved to attract attending ants, protecting the hosts, but it is unknown if EFNs on different plants have the same impact on the relations between an aphid species feeding on those plants and its tending ant. Experimental research was conducted to examine the attraction of Tapinoma erraticum scout ants to honeydew from the aphid Aphis gossypii feeding on two different plants, Prunus amygdalus and Mentha piperita, negligence of tending the aphids, and survival of the aphids in the presence of artificial EFNs. The scout ants were significantly more attracted to artificial nectar dispensed on P. amygdalus leaves than on M. piperita, or aphids on both plants and water. They neglected aphids in the presence of artificial EFNs on M. piperita but not on P. amygdalus. The aphid population on M. piperita did not statistically change in the presence of artificial EFNs during the 8 days of the third experiment. On P. amygdalus, the aphids succeeded in developing fully to winged form. In conclusion, the responses of the ants tending aphids to the presence of artificial EFNs were influenced by the host plant.     

Variation in social organization influences the opportunity for sexual selection in a social lizard

Social monogamy has traditionally been suggested to be maintained because of weak sexual selection on male partner acquisition. However, the ubiquitous incidence of extra-pair paternity suggests that sexual selection can be strong in monogamous systems, although studies partitioning variance in male reproductive success have come to mixed conclusions. Here, we use detailed field data to examine variance in male reproductive success and its implications for the maintenance of sociality in a population of the socially monogamous lizard Egernia whitii. We show that both within-pair and, to a lesser extent, extra-pair partner acquisition contribute to the variance in male reproductive success, resulting in considerable opportunity for sexual selection. Despite this, levels of multiple mating are lower in Egernia compared to other reptiles, suggesting that male partner acquisition is constrained. We suggest that this constraint may be a result of strong territoriality combined with sexual conflict over multiple mating generated by costs of extra-pair paternity to females as a result of facultative male care. This has the potential to limit sexual selection by reducing variance in male reproductive success and therefore contribute to the maintenance of complex social organization.     

Ant attendance reduces flight muscle and wing size in the aphid Tuberculatus quercicola

In otherwise mutualistic relationships between aphids and ants, attendance by ants often has negative impacts on aphids. For example, in a previous study using traps in the field, the aphid Tuberculatus quercicola, which exhibits mutualistic interactions with ants, showed extremely low dispersal rates, despite having long wings. This study investigates whether components of the flight apparatus (mesonotum length, flight muscle and wings) differ between aphids attended by ants and not attended by ants. Randomized block analysis of variance, using body length as a covariate, showed that ant attendance has a negative influence on aphid flight apparatus. This result indicates that aphids produce honeydew at the expense of resource investment in flight apparatus. Since the dispersal of T. quercicola is limited under ant attendance, the reduction in flight apparatus could precede a decrease in body size. This study also showed that flight apparatus was more developed in aphids under ant-exclusion conditions. This may imply that T. quercicola fly when ants are not available. The maintenance of flight apparatus in T. quercicola might therefore be partly explained by gene flow on the rare occasions that this aphid species disperses.     

Soldier differentiation during embryogenesis of a social aphid, Pseudoregma bambucicola

To understand the developmental process of aphid soldier differentiation, we investigated the morphological characters of normal nymphs, soldier nymphs and developing embryos of Pseudoregma bambucicola. Results of morphometric analyses showed that normal and soldier nymphs formed discrete clusters on the basis of several morphological characters, although a small number of intermediate individuals, termed ‘intercaste nymphs’, were present. In late embryonic stages, normal and soldier embryos were morphologically distinguishable. The earlier the embryonic stage, the smaller the morphological differences between them. In early embryos less than 1000 µm in length, normal and soldier embryos were not morphologically distinguishable, suggesting that the onset of soldier differentiation occurs at an early embryonic stage. Throughout embryonic development, morphological differentiation of the soldier caste proceeded gradually. Notably, several morphological characters of soldiers grew remarkably upon larviposition. Observation of embryonic leg cuticle revealed a characteristic folding structure, indicating that some morphological traits of the soldier are exaggerated upon larviposition through expansion of the folded cuticle. We suggest that morphological differentiation of the soldier caste in P. bambucicola comprises two phases: gradual growth during embryogenesis and rapid growth upon larviposition.     

Ant tending impairs performance of Aenasius bambawalei by manipulating the honeydew composition produced by Phenacoccus solenopsis

Honeydew produced by hemipterans is known as a possible kairomonal resource for parasitoids. The application of artificial honeydew effectively improves the performance of natural enemies. Aenasius bambawalei is a particularly dominant and aggressive endoparasitoid of the invasive mealybug Phenacoccus solenopsis. Our previous study showed that tending by the ghost ant Tapinoma melanocephalum significantly reduced the parasitism of A. bambawalei. We hypothesize that ghost ant tending influences host location of parasitoids by manipulating the composition of the honeydew produced by mealybugs. In this study, we tested whether the honeydew composition differs between treatments with and without ant attendance and whether changes in the honeydew influence the performance of A. bambawalei. Our results show that the sucrose concentration increased significantly in the ant‐attendance treatment but decreased when ant attendance was switched to an ant‐exclusion treatment; the inverse was true for the glucose concentration. Compared with the plastic honeydew treatment (mealybug with ant attendance), parasitoids spent much more time searching, had longer lifespans and showed higher parasitism on filter papers treated with natural honeydew (mealybug without any pre‐treatment) and those treated with convalescent honeydew (mealybug having experienced ant attendance and then switched to ant exclusion). These results support the hypothesis that ant tending influences the performance of parasitoids by manipulating honeydew composition.     

From maternal tending to adolescent befriending: The adolescent transition of social support

Attachment theory holds that parental relationships have lifelong effects on offspring social lives. The tend-and-befriend hypothesis posits that female friendships among humans evolved as part of a primate-wide coping mechanism to mediate stress by relying on social support. Here we bridge developmental and evolutionary frameworks to examine adolescent girls’ perception of their reliance on female friendship for social support, how perceptions of parental relationships affect peer relationships, and the extent to which parent and peer relationships buffer depressive symptoms. We predict perceived maternal relationship quality will be positively associated with close female friendships, and maternal relationships, paternal relationships, and female friendship will buffer depressive symptoms. Participants were adolescent girls from a summer science camp (N = 95). Participants filled out demographic information, social network surveys, the Parent-Adolescent Communication Scale, and the Center for Epidemiology Depression Scale. Data was analyzed with Pearson's correlations, t tests, and path analysis. Adolescent girls with few female friends, compared with girls who had more than two very close female friends, experienced more depressive symptoms (t = 3.382, p = .001, D = 0.784). Adolescent girls with few female friends experienced more depressive symptoms compared to girls with two or more very close female friends (t = 3.382, p = .001, D = 0.784). Stronger maternal and paternal relationships were associated with having more female friends (maternal: t = −3.213, p = .003, D = 0.837; paternal: t = −2.432; p = .017). In the path analysis model, only maternal relationship quality significantly predicted female friendship category (β = .33, CR = 2.770, p < .006). Furthermore, participants with two or more very close female friends and higher paternal relationship quality had significantly fewer depressive symptoms (friends; β = −.19, CR = −2.112, p = .035; paternal: β = −.33, CR = −3.220, p < .001), and older participants had more depressive symptoms (β = .17, CR = −1.931, p = .036). These results provide additional support for the tend-and-befriend hypothesis, suggesting that maternal tending sets the stage for close female friendships.