Competitive interactions between parasitoid larvae and the evolution of gregarious development

We report experiments using two closely related species of alysiine braconids directed at understanding how gregarious development evolved in one subfamily of parasitoid wasps. Theoretical models predict that once siblicide between parasitoid wasps has evolved, it can only be lost under stringent conditions, making the transition from solitary to gregarious development exiguous. Phylogenetic studies indicate, however, that gregariousness has independently arisen on numerous occasions. New theoretical models have demonstrated that if gregarious development involves reductions in larval mobility, rather than a lack of fighting ability (as in the older models), the evolution of gregariousness is much more likely. We tested the predictions of the older tolerance models (gregariousness based on non-fighting larval phenotypes) and the reduced mobility models (gregariousness based on non-searching larval phenotypes) by observing larval movement and the outcome of interspecific competition between Aphaereta genevensis (solitary) and A. pallipes (gregarious) under multiparasitism. Differences in larval mobility matched the prediction of the reduced mobility model of gregarious development, with the solitary A. genevensis having larvae that are much more mobile. The proportion of hosts producing the solitary species significantly declined after subsequent exposure to females of the gregarious species. This contradicts the prediction of the older models (fighting vs non-fighting phenotypes), under which any competitive interactions between solitary and gregarious larvae will result in a highly asymmetrical outcome, as the solitary species should be competitively superior. The observed outcome of interspecific competition offers evidence, with respect to this subfamily, in favour of the new models (searching vs non-searching phenotypes).     

Gregariousness and repellent defences in the survival of phytophagous insects

Group living has both costs and benefits for plant‐feeding insects, but defence against predators is the most widely acknowledged benefit. Gregarious folivores typically have warning coloration and elaborate anti‐predator defences. Do these defences protect these species from predation? To see if protection from predators generally results from gregariousness, I compared the shapes of published survivorship curves of externally feeding, gregarious and solitary Lepidoptera and Symphyta. Gregarious species are less likely than solitary species to die in the larval stages. However, solitary species that have anti‐predator defences do not have higher larval survival compared to gregarious species. This result, along with evidence from experimental manipulations of group size, suggests that repellent defences per se do not increase survival of gregarious larvae. Group behaviour is undoubtedly important in affecting the higher larval survival of gregarious species, but we currently cannot determine whether predator learning, dilution of risk, or rapid development contribute most to increasing survival.     

Linking spatial processes to life-history evolution of insect parasitoids

Understanding the evolutionary transition from solitary to group living in animals is a profound challenge to evolutionary ecologists. A special case is found in insect parasitoids, where a tolerant gregarious larval lifestyle evolved from an intolerant solitary ancestor. The conditions for this transition are generally considered to be very stringent. Recent studies have aimed to identify conditions that facilitate the spread of a gregarious mutant. However, until now, ecological factors have not been included. Host distributions and life-history trade-offs affect the distribution of parasitoids in space and thus should determine the evolution of gregariousness. We add to current theory by using deterministic models to analyze the role of these ecological factors in the evolution of gregariousness. Our results show that gregariousness is facilitated through inversely density-dependent patch exploitation. In contrast, host density dependence in parasitoid distribution and patch exploitation impedes gregariousness. Numerical solutions show that an aggressive gregarious form can more easily invade a solitary population than can a tolerant form. Solitary forms can more easily invade a gregarious, tolerant population than vice versa. We discuss our results in light of exploitation of multitrophic chemical cues by searching parasitoids and aggregative and defensive behavior in herbivorous hosts.     

Understanding gregariousness in a larval Lepidopteran: the roles of host plant, predation, and microclimate

Abstract.  1. Many moth and butterfly larvae are gregarious early in development, but become solitary in late instars. This ontogenetic variation in behaviour is probably the result of temporal changes in the costs and benefits associated with gregariousness. This study provides observational and experimental evidence that, in one particular moth species, a series of different ecological factors influence larval behaviour at different times during development.
2. Field observations show that young caterpillars of the limocodid Doratifera casta form large aggregations while foraging, but that mature larvae are largely solitary.
3. A field experiment revealed that individual first to third instar larvae in larger groups develop more rapidly, but that group size had no detectable influence on survival. The developmental advantage associated with gregariousness is affected by host plant species, but not by predator exclusion, suggesting that group living in these cryptic early instar larvae promotes feeding facilitation, but does not provide individuals with protection from natural enemies.
4. Laboratory experiments revealed that aposematic fourth instar caterpillars in large groups were less likely to be attacked by a generalist insect predator than those in small groups.
5. Field observations provided no evidence that group living affects body temperature, suggesting that microclimatic factors do not favour gregariousness in this species.
6. It is concluded that gregariousness in D. casta confers at least two different advantages on larvae at different stages early in development, but that these advantages disappear, or are outweighed by costs associated with intraspecific competition, in final instars.     

Complementary sex determination in the parasitoid wasp Cotesia vestalis (C. plutellae)

In the Hymenoptera, single locus complementary sex determination (sl-CSD) describes a system where males develop either from unfertilized haploid eggs or from fertilized diploid eggs that are homozygous at a single polymorphic sex locus. Diploid males are often inviable or sterile, and are produced more frequently under inbreeding. Within families where sl-CSD has been demonstrated, we predict that sl-CSD should be more likely in species with solitary development than in species where siblings develop gregariously (and likely inbreed). We examine this prediction in the parasitoid wasp genus Cotesia, which contains both solitary and gregarious species. Previous studies have shown that sl-CSD is absent in two gregarious species of Cotesia, but present in one gregarious species. Here, we demonstrate CSD in the solitary Cotesia vestalis, using microsatellite markers. Diploid sons are produced by inbred, but not outbred, females. However, frequencies of diploid males were lower than expected under sl-CSD, suggesting that CSD in C. vestalis involves more than one locus.     

Mothers' Egg-pooling and Aposematic Offspring's Gregariousness: Cui bono?

Recently Sillén-Tullberg & Leimar (1988) modelled a general explanation for the evolution of gregariousness in prey organisms that live exposed, have no means of escape when discovered by a predator, and are small in relation to a potential predator (who thus can sample many prey individuals in one encounter). The model predicts that gregarious prey organisms of that type ought to be distasteful, and that the evolution of gregariousness will be favoured by aposematic coloration facilitating avoidance learning in a predator. Obviously, any protective power of grouping depends on group size. According to the Sillén-Tullberg & Leimar model, (1) “members of small groups may have a higher rate of death from predation than solitary individuals, but above a certain minimum group size, group members do better than solitary individuals; … as group size increases above the minimum value, group members suffer fewer and fewer deaths from predation”. They benefit from the “decreased risk of predator attack on any particular individual”, called dilution effect. (2) “The more prey specimens that the predator needs to sample during avoidance learning, the larger an aggregation needs to be in order for gregariousness to be advantageous”. It is further explained that (3) selection resulting from predation favours increase in group size until it “acts like a predator-satiation mechanism”.     

The role of larval aggression and mobility in the transition between solitary and gregarious development in parasitoid wasps

Models explaining the appearance of gregariousness in insect parasitoids assume the presence of a tolerance gene that enables nonsiblicidal behaviour in gregarious larvae. Under this assumption, nontolerant individuals should attack and kill tolerant individuals when sharing a host, making this behaviour susceptible to invasion by nontolerant individuals. We propose an alternative hypothesis where gregarious larvae retain their aggressiveness but are less mobile. We tested this hypothesis with two sympatric and congeneric species of Mymaridae, Anaphes victus and Anaphes listronoti , respectively, solitary and gregarious egg parasitoids of a Curculionidae, Listronotus oregonensis . Results obtained in competition experiments and from direct observation of movement in mymariform larvae of both species support the reduced mobility hypothesis. By being immobile while retaining their fighting capacity, A. listronoti mymariform larvae appear to optimize host utilization through gregarious development, but can still defend themselves against sympatric aggressive species.     

Why some rails have white tails: the evolution of white undertail plumage and anti-predator signaling

Conspicuous plumage patches have evolved in birds as conspecific signals for mate attraction and assessment, intersexual competition or to signal alarm. Signals may alternatively be directed at potential predators to discourage pursuit. Rails (Family Rallidae) are ground-dwelling birds, many of which inhabit wetlands, while others occur in forests and grasslands. They are renown for their secretive nature and the tendency to flick their tails when observed. This behavior is more conspicuous in species with white undertail coverts that contrast sharply with darker body plumage. Using species comparisons and controlling for phylogeny, we investigated four hypotheses for the evolution of white undertail coverts in rails. We found little support for the hypothesis that white tails are sexually selected: white tails were not more common in species with polygamous as opposed to monogamous mating systems, species with sexual dimorphism, nor species that display their tails in courtship. Nor did our results support the hypothesis that white tail plumage evolved for intersexual competition during territorial interactions. Instead, we found that species that flock for at least part of the year and species found in open as opposed to concealing habitats were significantly more likely to have white undertail coverts. Rail species inhabiting concealing habitats are less commonly gregarious and more likely selected for crypsis. Using phylogenetically-controlled statistical inference we found that adaptation to open wetland habitats significantly precedes the evolution of white undertails, whereas gregariousness likely evolved later in some lineages. The inferred order of trait evolution suggests that this plumage characteristic could have been selected primarily for enhancement of an anti-predator signal rather than a social signal for conspecifics.     

Variation in hydraulic architecture and gas-exchange in two desert sub-shrubs,<Emphasis Type="Italic"> Hymenoclea salsola</Emphasis> (T. &; G.) and<Emphasis Type="Italic"> Ambrosia dumosa</Emphasis> (Payne)

Adjustment of hydraulic architecture in response to environmental conditions was studied in two warm-desert sub-shrubs, Hymenoclea salsola and Ambrosia dumosa, both at the level of genetic adaptation along a climatic gradient and plastic response to immediate growth conditions. Individuals of both species originating from southern populations developed higher leaf-specific hydraulic conductance in the common greenhouse than individuals from northern populations. Hydraulic conductance was higher in plants grown at high temperature, but did not vary as a function of growth relative humidity. Hydraulic conductance was not correlated within species with individual variation in vessel diameter, cavitation vulnerability, or root:shoot ratio, but was strongly, negatively correlated with the fraction of total plant biomass allocated to leaves. For both species, stomatal conductance (g _s) at high leaf-to-air vapor pressure difference (ν) was tightly correlated with variability in hydraulic conductance, as was the sensitivity of stomatal closure to increasing ν. Experimentally increasing shoot water potential by soil pressurization, under conditions where high ν had already caused stomatal closure, led to substantial stomatal reopening in both species, but recovery was significantly higher in H. salsola. Hydraulic conductance was higher in H. salsola than A. dumosa. H.salsola also differed from A. dumosa by being a representative of a highly specialised group of desert shrubs which use the twigs as a major photosynthetic organ. The southern population of H. salsola produced far fewer leaves and relied much more heavily on twig photosynthesis than the northern population. At the whole-plant level, increased reliance on twig photosynthesis was associated with higher leaf-specific hydraulic conductance, but equivalent whole-plant photosynthesis on either a dry weight (μmol CO₂ g^–1) or nitrogen basis (μmol CO₂ g^–1)). This suggests that twig photosynthesis might be one way of increasing hydraulic conductance per unit photosynthetic canopy by increasing allocation to an organ which simultaneously performs photosynthetic, support, and transport functions. Received: 13 December 1999 / Accepted: 31 March 2000     

Aggregation, defence and warning signals: the evolutionary relationship

In a seminal contribution, Fisher argued how distastefulness could incrementally evolve in a prey species that was distributed in family groups. Many defended prey species occur in aggregations, but did aggregation facilitate the evolution of defence as Fisher proposed or did the possession of a defence allow individuals to enjoy the benefits of group living? Contemporary theory suggests that it can work both ways: pre-existing defences can make the evolution of gregariousness easier, but gregariousness can also aid the evolution of defence and warning signals. Unfortunately, the key phylogenetic analyses to elucidate the ordering of events have been hampered by the relative rarity of gregarious species, which in itself indicates that aggregation is not a pre-requisite for defence. Like the underlying theory, experimental studies have not given a definitive answer to the relative timing of the evolution of defence and aggregation, except to demonstrate that both orderings are possible. Conspicuous signals are unlikely to have evolved in the absence of a defence and aggregated undefended prey are likely to be vulnerable to predation in the absence of satiation effects. It therefore seems most likely that defence generally preceded the evolution of both aggregation and signalling, but alternative routes may well be possible.     

Group connection and the number of males in female-philopatric animal groups

Previous studies have considered the equilibrium group size in gregarious animal species assuming isolated groups. Neighboring groups usually interact, which likely affects the equilibrium group size. Here I examine the possibility that the movements of solitary males between areas near neighboring groups cause the number of group males to increase in female-philopatric animal species when groups are connected. I hypothesized the following mechanisms. In habitats where groups are connected, solitary males move easily between areas near adjacent groups. Group males will accept one solitary male as a new member. Another solitary male migrates from an area near the group to an area near a neighboring group defended by relatively fewer group males. The model predicts that the number of group males increases through the hypothesized mechanisms when groups are connected if group males and solitary males do not cooperate effectively.     

Comparison of gregariousness in larvae and adults of four species of zetoborine cockroaches

Insects observed in groups in nature may be gathered either by attractants from the environment or by conspecifics. Field distribution data alone are thus insufficient to assess congregation by conspecifics and complementary laboratory tests of spacing patterns are required. Such tests were performed in four species of Zetoborinae (Insecta, Blattaria), for which field studies showed differences in spatial distribution (Schultesia lampyridiformis Roth, Phortioeca nimbata Burmeister, Lanxoblatta emarginata Burmeister and Thanatophyllum akinetum Grandcolas). Gregariousness, mobility, and sticking to shelters were compared between these four species. Tests were performed on pairs of adults of the same sex and opposite sexes, and also on first instar larvae, either in isolation or in groups of two and four individuals. In S. lampyridiformis, adults were strongly gregarious, whereas larvae dispersed early after birth and were very mobile during the first instar. In P. nimbata, larvae and adults were gregarious, while in L. emarginata larvae were weakly gregarious, and gregariousness decreased when density increased. Adults of L. emarginata seemed to be indifferent to each other. Larvae and adults of T. akinetum were solitary and they actively dispersed. The varying levels of gregariousness among species are discussed according to the known ecological habits in Zetoborinae.     

Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding Macrolepidoptera: a phylogenetic analysis based on independent contrasts

Gregariousness in insects is often associated with aposematism, which has two distinct properties, repellent defence and warning coloration. Theoretically, both repellent defence and warning coloration are expected to facilitate the evolution of gregariousness. This paper investigates whether the likelihood for gregariousness to evolve is higher (1) in the presence of chemical/physical defence and (2) in the presence of warning coloration, in a sample of over 800 tree-living macrolepidopteran species. A new phylogenetic technique for investigating the correlation between two discrete characters, based on independent contrasts, is used. For each of nine contrasts, based on presence/absence of repellent defence that included transitions to gregariousness, the frequency of such transitions was highest in the lineage with repellent defence present. Similarly, out of 12 contrasts based on presence/absence of warning coloration 10 had the highest frequency of transitions to gregariousness in the lineage with warning coloration. Thus, gregariousness is more likely to evolve in lineages with repellent defence and in lineages with warning coloration, but it is concluded that, since these traits are strongly intercorrelated, it is very difficult to distinguish between their separate effects on the evolution of gregariousness. Our findings indicate, however, that potentially, the presence of repellent defence may be sufficient for the evolution of gregariousness.     

Gregarious settlement in cypris larvae:the effects of cyprid age and assay duration

Gregarious behaviour of marine larvae is perhaps most clearly associated with finding a suitable habitat in a changeable or restricted environment, or with finding other conspecifics with which to mate. Prior work has shown that in settlement assays using cypris larvae of the barnacle Balanus amphitrite, gregarious interactions significantly affected the interpretation of experiments testing the activity of organic settlement promoters and inhibitors. Other studies have also shown effects of cyprid age and pheromone concentration on settlement behaviour. However, the effects of interactions between gregariousness and these two factors are not known. The aim of this study was to test the hypotheses that i) as cyprids age the effects of gregariousness become less apparent, and ii) as the duration of the experiment increases gregarious effects become more apparent, using cypris larvae of B. amphitrite and Balanus improvisus. Three age classes of cyprids were used at six densities in a fully factorial design. For B. improvisus cyprids significant gregarious effects occurred between 3 or more larvae, and although larval age and experiment duration had significant main effects, there were no interactions between these important factors and gregariousness. For B. amphitrite cyprids significant gregarious effects also occurred with 3 larvae per well, though this effect was strongly dependent upon experiment duration. B. amphitrite cyprid sensitivity to conspecific cues does not change with age, although increasing experiment duration and age interact to increase settlement. Differences between species may be due to different thresholds to conspecific larval cues, or B. improvisus cyprids release much more larval temporary adhesive during exploration.     

How feeding competition determines female chimpanzee gregariousness and ranging in the Taï National Park, Côte d'Ivoire

Socioecological theory suggests that feeding competition shapes female social relationships. Chimpanzees (Pan troglodytes) live in fission–fusion societies that allow them to react flexibly to increased feeding competition by forming smaller foraging parties when food is scarce. In chimpanzees at Gombe and Kibale, female dominance rank can crucially influence feeding competition and reproductive success as high‐ranking females monopolize core areas of relatively high quality, are more gregarious, and have higher body mass and reproductive success than low‐ranking females. Chimpanzee females in Taï National Park do not monopolize core areas; they use the entire territory as do the males of their community and are highly gregarious. Although female chimpanzees in Taï generally exhibit a linear dominance hierarchy benefits of high rank are currently not well understood. We used a multivariate analysis of long‐term data from two Taï chimpanzee communities to test whether high‐ranking females (1) increase gregariousness and (2) minimize their travel costs. We found that high‐ranking females were more gregarious than low‐rankers only when food was scarce. During periods of food scarcity, high rank allowed females to enjoy benefits of gregariousness, while low‐ranking females strongly decreased their gregariousness. High‐ranking females traveled more than low‐ranking females, suggesting that low‐rankers might follow a strategy to minimize energy expenditure. Our results suggest that, in contrast to other chimpanzee populations and depending on the prevailing ecological conditions, female chimpanzees at Taï respond differently to varying levels of feeding competition. Care needs to be taken before generalizing results found in any one chimpanzee population to the species level. Am. J. Primatol. 73:305–313, 2011. © 2010 Wiley‐Liss, Inc.     

Gregariousness increases brain size in ungulates

The brain’s main function is to organise the physiological and behavioural responses to environmental and social challenges in order to keep the organism alive. Here, we studied the effects that gregariousness (as a measurement of sociality), dietary habits, gestation length and sex have on brain size of extant ungulates. The analysis controlled for the effects of phylogeny and for random variability implicit in the data set. We tested the following groups of hypotheses: (1) Social brain hypothesis—gregarious species are more likely to have larger brains than non-gregarious species because the former are subjected to demanding and complex social interactions; (2) Ecological hypothesis—dietary habits impose challenging cognitive tasks associated with finding and manipulating food (foraging strategy); (3) Developmental hypotheses (a) energy strategy: selection for larger brains operates, primarily, on maternal metabolic turnover (i.e. gestation length) in relation to food quality because the majority of the brain’s growth takes place in utero, and finally (b) sex hypothesis: females are expected to have larger brains than males, relative to body size, because of the differential growth rates of the soma and brain between the sexes. We found that, after adjusting for body mass, gregariousness and gestation length explained most of the variation in brain mass across the ungulate species studied. Larger species had larger brains; gregarious species and those with longer gestation lengths, relative to body mass, had larger brains than non-gregarious species and those with shorter gestation lengths. The effect of diet was negligible and subrogated by gestation length, and sex had no significant effect on brain size. The ultimate cause that could have triggered the co-evolution between gestation length and brain size remains unclear.     

Host range in solitary versus gregarious parasitoids: a laboratory experiment

Behavioural interactions among relatives may have consequences for many other traits. We tested the hypothesis that solitary parasitoids (displaying siblicidal behaviour in their larvae) have narrower host ranges than gregarious parasitoids (with tolerant larvae). In laboratory experiments, we compared parasitization success in two sister species of braconid wasp [Aphaereta genevensis (Fischer), solitary, and Aphaereta pallipes (Say), gregarious (Hymenoptera: Braconidae: Alysiini)] on eight Drosophila species or strains. Host species or strain was the most important factor affecting parasitization success, and some of this variation was accountable to host physiological defences. Although two hosts were more suitable for the solitary species, and one more suitable for the gregarious species, these differences were small, and there was no consistent difference across all hosts. Wasp body size was positively correlated with parasitization success in both wasp species. This may be because body size increases oviposition success, or the motivation to oviposit. In A. pallipes parasitization success peaked after 3–4 days, but later in A. genevensis. This is likely due to low life expectancy and high egg loads increasing oviposition tendency in young A. pallipes, and egg limitation decreasing oviposition tendency in old A. pallipes. These data suggest that interactions among wasp larvae do not greatly affect the size of the fundamental niche examined here. However, they show the potential for life history traits, which differ between the species as a likely consequence of larval interactions, to affect the extent of the realized niche.     

Sociality, density-dependence and microclimates determine the persistence of populations suffering from a novel fungal disease, white-nose syndrome

Disease has caused striking declines in wildlife and threatens numerous species with extinction. Theory suggests that the ecology and density-dependence of transmission dynamics can determine the probability of disease-caused extinction, but few empirical studies have simultaneously examined multiple factors influencing disease impact. We show, in hibernating bats infected with Geomyces destructans, that impacts of disease on solitary species were lower in smaller populations, whereas in socially gregarious species declines were equally severe in populations spanning four orders of magnitude. However, as these gregarious species declined, we observed decreases in social group size that reduced the likelihood of extinction. In addition, disease impacts in these species increased with humidity and temperature such that the coldest and driest roosts provided initial refuge from disease. These results expand our theoretical framework and provide an empirical basis for determining which host species are likely to be driven extinct while management action is still possible.     

A Comparison of Behavioral Interactions in Solitary and Presocial Zetoborinae Cockroaches (Blattaria,Blaberidae)

The social behavior of five species of Zetoborinae cockroaches is compared with respect to inter-individual interactions of nymphs in the laboratory. These species belong to the same Neotropical subfamily and were characterized as gregarious (Lanxoblatta emarginata, Parasphaeria boleiriana, Phortioeca nimbata, Schultesia lampyridiformis) and solitary (Thanatophyllum akinetum) by previous field studies. Our results show that gregarious species accept closer contacts than does the solitary one. The solitary species did not display especially short, infrequent or less diverse behavioral sequences when forced to remain aggregated, but its interactions are characterized by fewer acts promoting contact and more dominance-like acts. The solitary species symmetrically interacts with conspecifics and does not show specific dispersal-promoting behaviors. This suggests that the solitary behavior observed in the field for species of Zetoborinae mainly results from a passive spacing tendency and a lack of attraction for conspecifics. One of the gregarious species, P. boleiriana, was previously described as subsocial with nymphs remaining with the female in a wood chamber after brood birth. This species does not show a peculiar behavioral repertoire but its interactions are characterized by more dominance-like behaviors than are those of the non-subsocial gregarious species. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.