Phenotypic variation in male and worker encapsulation response in the bumblebee Bombus terrestris

Abstract.  1. Life-history traits such as immunity are often characterised by the presence of large phenotypic variation, but it often remains unclear how and why this variation is maintained by selection.
2. Here an annual social insect, the bumblebee Bombus terrestris , was used to study variation in encapsulation response of males and workers. Bumblebees are a suitable system to study offspring immunity because they are host to a broad variety of different parasites. Bumblebee males, in particular, have a long lifespan compared with other social insect males and their immunity should therefore be an important element for colony reproductive success.
3. Encapsulation response, which was used here as a measurement for the generalised immune defence capacity of an individual, was found to be a highly variable trait. High levels of worker response correlated with low levels of colony parasitism rates.
4. Encapsulation response was found to be (a) lower in males compared with sister workers, and (b) lower in late-produced cohorts compared with early ones.
5. In colonies with delayed sexual reproduction, males had a lower encapsulation response. Thus, investments into immunity seemed reduced in later male cohorts and those eclosing later in the season, perhaps because males had a shorter expected remaining time to acquire matings. The results presented add further evidence that immune defence is a key variable defining colony fitness in social insects.     

Greater cuticular melanism is not associated with greater immunogenic response in adults of the polymorphic mountain stone weta, Hemideina maori

Abstract.  1. Greater immune function is associated with the high-density melanic phase of polyphenic insects, appearing to compensate for density-dependent increases in susceptibility to parasites and/or pathogens. Other types of discrete variation in cuticular colour occur in insects (which may or may not be associated with melanin pigmentation), but whether this variation is predictive of immune ability has not been investigated.
2. In the mountain stone weta Hemideina maori , a black morph and yellow banded morph occur. These morphs are not seasonally polyphenic and have discrete haplotype genetic markers. Black individuals are typically found at lower local densities than yellow individuals, contrary to relations between cuticular melanism and density seen in polyphenic insects.
3. Yellow males and females had greater melanotic encapsulation responses upon immune challenge than did black males and females, but these differences were not associated with differences in temperature selection between morphs. Morph differences in melanotic encapsulation responses were somewhat related to differences between morphs in haemocyte concentrations.
4. These results indicate that a common form of immune expression is not heightened with dark coloration in the mountain stone weta. Thus, earlier findings of greater immunity associated with darker cuticles in phase polyphenic insects cannot be extended to insects with other forms of discrete colour variation. These findings will help in elucidating causes and consequences of such colour polymorphism, which is widespread in several insect orders.     

Immunity and reproduction during colony foundation in the dampwood termite, Zootermopsis angusticollis

Abstract.  Termite primary reproductives may be exposed to pathogens when dispersing from their parental nest and establishing a new colony. Immunity and reproduction are investigated during colony foundation by implanting a nylon filament into the abdomen of mated and unmated female and male primary reproductives of the dampwood termite Zootermopsis angusticollis. Primary reproductives are paired in combinations of female/male, female/female and male/male and, using confocal microscopy, immune defence is assessed by measuring the degree of encapsulation of nylon implants during three periods of colony foundation: (I) shortly after pairing; (II) during copulation/oocyte maturation; and (III) during oviposition. There are differences in the encapsulation response of mated and unmated termites that are contingent on the period of colony foundation when termites are challenged. Mated females and males have significantly greater encapsulation responses than their unmated counterparts shortly after pairing, perhaps as a prophylactic measure against exposure to disease. The encapsulation response of mated and unmated males does not differ significantly during periods II and III. The onset of oviposition is significantly delayed in mated females that received implants during periods I and II. Mated females have a significantly reduced encapsulation response during the time of copulation and oocyte maturation, but not during oviposition. Overall, males have a significantly greater ability than females to encapsulate a nylon implant. The findings suggest that reproduction can reduce the immune response in female primary reproductives. The results are discussed in light of trade-offs between immunity and reproduction during the critical life-history phase of colony establishment in termites.     

Can life‐history and defence traits predict the population dynamics and natural enemy responses of insect herbivores?

Abstract.  1. Life-history differences between herbivorous insects with eruptive and latent population dynamics are potentially useful for predicting population size variability. An association has also been demonstrated between herbivorous insect defence traits and the responses of various natural enemies.
2. Here predictions of population dynamics and natural enemy responses based on life-history and defence traits are tested using Gonometa postica Walker and G. rufobrunnea Aurivillius, two Southern Hemisphere Macrolepidoptera (Lasiocampidae) species. The temporal and spatial variation in pupal abundance and patterns of pupal parasitism and predation for both species are described and quantified for the first time.
3. Eleven sites were sampled over four generations across the region where both species have historically reached high population densities. Although there was evidence suggesting that population synchrony is driven by weather patterns, site-specific environmental differences contributed to the observed population variability. This study is the first to quantify the extent of population size variability of a species with an intermediate position on the eruptive–latent population dynamic gradient, where data on insect population dynamics is scarce.
4. Support for the life-history–population dynamic relationship was found, as intermediate population size variability for these species was observed. Larval and pupal defence traits, however, were poor and inconsistent predictors of mortality rate. Pupal cocoon structure differences, previously documented for these Gonometa species, may in fact explain the interspecific differences in natural enemy responses found.
5. Predicted population dynamics and natural enemy responses may, however, be overridden by ecological conditions. Nevertheless, life-history and defence traits provide a useful basis for predicting population dynamics of poorly studied species.     

A test of life-history theories of immune defence in two ecotypes of the garter snake, Thamnophis elegans

1.  Life-history theorists have long observed that fast growth and high reproduction tend to be associated with short life span, suggesting that greater investment in such traits may trade off with self-maintenance. The immune system plays an integral role in self-maintenance and has been proposed as a mediator of life-history trade-offs.
2.  Ecoimmunologists have predicted that fast-living organisms should rely more heavily on constitutive innate immunity than slow-living organisms, as constitutive innate defences are thought to be relatively inexpensive to develop and can provide a rapid, general response to pathogens.
3.  We present the first study to examine this hypothesis in an ectothermic vertebrate, by testing for differences in three aspects of constitutive innate immunity in replicate populations of two life-history ecotypes of the garter snake Thamnophis elegans , one fast-living and one slow-living.
4.  As predicted, free-ranging snakes from the fast-living ecotype had higher levels of all three measures of constitutive innate immunity than the slow-living ecotype. These differences in immunity were not explained by parasite loads measured. Furthermore, both ecotypes exhibited a positive relationship between innate immunity and body size/age, which we discuss in the context of ectotherm physiology and ecotype differences in developmental rates.     

Bottom-up cascading effects in a tritrophic system: interactions between plant quality and host-parasitoid immune responses

Abstract.  1. Little is known about underlying mechanisms by which plants indirectly affect parasitism success in hymenopteran endoparasitoids. The hypothesis that host-plant effects can challenge the innate immune system of an insect host was experimentally tested in this study using a model tritrophic, crucifer – lepidopteran [ Plutella xylostella (L.)] – parasitoid [ Cotesia plutellae (Kurdjumov)], system.
2. The effects of host-plant suitability on herbivore performance and parasitism were examined. The bottom-up effect of plant suitability on host-parasitoid immune responses was then evaluated using measures of cellular and humoral effectors.
3. Host-plant quality showed a significant effect on the encapsulation response of P. xylostella to first instar but not to second instar parasitoid larvae. Encapsulation was never sufficient to prevent parasitoid emergence.
4. Poor host-plant suitability suppressed phenoloxidase activity in the absence of the parasitoid. The suppressive effect of C. plutellae on phenoloxidase activity was much greater and no plant effects were detectable after insects had been parasitized.
5. Despite strong plant effects on parasitism, those on immune effectors of the host were transitory or overwhelmed by the effect of the parasitoid.
6. These results demonstrated that plant-mediated variation in parasitism success by C. plutellae were not as a result of plant nutritional status or other attributes affecting the immune function of P. xylostella , nor to host-plant effects on superparasitism.
7. In these experiments, P. xylostella was a fully permissive host to C. plutellae and host-plant-mediated effects on the innate immune response appeared to play no part in parasitoid survival within hosts.     

Senescence of immune defence in Bombus workers

Abstract 1. Senescence in workers of social insects is a particularly intriguing life-history trait as the future fitness of workers relies primarily on age-dependent survival rate. The pattern of senescence of immune defence traits was investigated under laboratory conditions in workers of two bumble bees: Bombus terrestris and B. lucorum .
2. In both species, there was a significant decrease with age in the ability to encapsulate a foreign object (a global measure of the efficiency of immune systems). This pattern of senescence was observed in all colonies in B. terrestris (seven) and B. lucorum (eight) assayed, even though, for the latter, there was some heterogeneity among colonies.
3. In B. terrestris , two other measures of immune defence were taken: the relative percentage of fat body in the abdomen and the concentration of haemocytes (the immune defence cells). The quantity of fat body increased only slightly with age and there was no effect for the concentration of haemocytes. Interestingly, the concentration of haemocytes decreased strongly after an encapsulation response, regardless of the age of workers.
4. The importance of the senescence pattern observed for the immune defence traits is discussed in the context of the social biology of workers.     

Inbreeding and extreme outbreeding cause sex differences in immune defence and life history traits in Epirrita autumnata

Empirical studies in vertebrates support the hypothesis that inbreeding reduces resistance against parasites and pathogens. However, studies in insects have not found any evidence that inbreeding compromises immune defence. Here we tested whether one generation of brother-sister mating or extreme outbreeding (mating between two populations) have an effect on innate immunity and life history traits in the autumnal moth, Epirrita autumnata. We show that the effect of inbreeding on immune response differed between the sexes: whereas in females, inbreeding significantly reduced encapsulation response against nylon monofilament ability, it did not have a significant effect on male immune response. There were also differences in the correlation of the immune response with other traits: in females increased immune response was positively correlated with large size, whereas in males immune response increased with a reduction in development time. Immune response differed significantly among families in males but not in females, both for the inbreeding and extreme outbreeding experiments. In conjunction with the observed immune responses to inbreeding, these data suggest that in males genetic variation for immune response is largely additive or non-directional with respect to dominance, whereas in females variation is much reduced and consists of directional dominance variance. Further, we show that encapsulation response against nylon monofilament is associated with the resistance against real pathogens suggesting that this widely used method to measure the strength of immune defence in insects is also a biologically relevant method.     

Influence of atmospheric carbon dioxide enrichment on induced response and growth compensation after herbivore damage in Lotus corniculatus

Abstract 1. Plant growth and chemical defence compounds in four Lotus corniculatus genotypes exposed to factorial combinations of ambient and elevated carbon dioxide, and herbivory by caterpillars of Polyommatus icarus were measured to test the predictions of the carbon/nutrient balance hypothesis.
2. Shoot and root biomass, allocation to shoots versus roots, and carbon-based defence compounds were greater under elevated carbon dioxide. Pupal weight of P. icarus was greater and development time shorter under elevated carbon dioxide.
3. Herbivory decreased shoot growth relative to root growth and production of nitrogen-based defence (cyanide). Young leaves contained more defence compounds than old leaves, and this response depended on carbon dioxide and herbivory treatments (significant interactions).
4. Genotype-specific responses of plants to carbon dioxide and herbivory were found for the production of cyanide. Furthermore, maternal butterfly-specific responses of caterpillars to carbon dioxide were found for development time. This suggests the existence of genetic variation for important defence and life-history traits in plants and herbivores in response to rising carbon dioxide levels.     

On understanding seasonal increases in damselfly defence and resistance against ectoparasitic mites

Abstract.  1. Defence against parasites and pathogens can be essential, yet not all hosts respond similarly to parasitic challenge. Environmental conditions are thought to explain variation in host responses to parasites.
2.  Lestes forcipatus damselflies emerging later in the season have shown higher resistance to the mite, Arrenurus planus , than hosts emerging earlier. This study was undertaken to determine whether variation in environmental temperatures characteristic of early vs. late emergence times, degree or costs of mite parasitism, and/or size of newly emerged adults could explain seasonal variation in defence and resistance to ectoparasitic mites.
3. In this study damselflies from early vs. late emergence groups differed in size at emergence and mite intensity. In general, early hosts were larger and had more mites than later hosts. However only experimental temperatures experienced by damselflies at emergence influenced defence and resistance against mites and not host size or degree of parasitism.
4. More specifically, hosts from early and late emergence groups did not differ in defence and resistance when held at the same temperatures in incubators. Housing at a high temperature, indicative of later in the season, was associated with higher defence and resistance for damselflies from both early and late emergence groups.
5. These results indicate that daily temperatures in relation to emergence timing can account for seasonal increases in resistance for this temperate insect. Seasonal increases in resistance may be expected for other temperate insect–parasite associations and should have important implications for the phenology of parasites and for seasonal variation in parasite-mediated selection.     

Life-history, genotypic, and environmental correlates of clutch size in the Glanville fritillary butterfly

Abstract.  1. Glanville fritillary butterfly ( Melitaea cinxia ) females lay up to 10 clutches of 50–300 eggs in their lifetime. Clutch size is an important life-history trait as larval group size affects survival throughout larval development.
2. Two experiments were carried out in a large population cage in the field to investigate the life-history and environmental correlates of clutch size.
3. Clutch size decreased with the cumulative number of eggs laid previously, increased with both female body weight and the number of days between consecutive clutches.
4. Genotypic differences among females in the glycolytic enzyme phosphoglucose isomerase had a significant influence on clutch size, partly because females of particular genotypes were able to initiate oviposition earlier in the day and thereby take advantage of the most favourable environmental conditions for oviposition.
5. Factors influencing clutch size were partly different in two summers, indicating the modulating effect of prevailing environmental conditions on reproductive performance.     

Spatial and temporal variation in a suite of life-history traits in two species of wolf spider

Abstract.  1. Life-history traits and density were assayed in seven populations of two sympatric species of wolf spider for three consecutive years. The goal of the study was to quantify population dynamics and its relation to spatial and temporal life-history variation.
2. Adult female body size and fecundity varied significantly, among field sites and among years, in both species. Female spiders of both species differed in mean relative reproductive effort among sites, but not among years. The size of offspring was invariable, with no significant differences due to site or year.
3. All populations of both species tended to either decrease or increase in density during a given year and this was tightly correlated with changes in prey consumption rates.
4. Since life-history patterns are determined primarily by selection, it is concluded that size at sexual maturity for females is phenotypically plastic and responds to changes in prey availability. Offspring size however is not plastic and it is likely that other selection forces have determined offspring size. Temporal fluctuations in population size are correlated over a large area relative to dispersal capabilities for these species and conservation efforts for invertebrates must take this into consideration.     

Individual quality and age affect responses to an energetic constraint in a cavity-nesting bird

Individual variation in life-history trade-offs can be causedby differences in quality and age. We tested for individualvariation in parental investment in incubating tree swallows(Tacyhcineta bicolor) subjected to a feather-clipping manipulation.Individual quality influenced how females were affected by featherclipping; lower quality clipped females showed a greater reductionin incubation and a greater loss of body condition than higherquality clipped females compared with controls. Most importantly,responses during incubation influenced nestling traits; lowerquality clipped females, particularly those losing the mostbody mass, raised nestlings in the poorest condition. Therewas no difference in incubation patterns of control females,but older clipped females suffered self-maintenance costs andraised offspring in better condition. In contrast, younger clippedfemales passed costs on to offspring through lower egg temperaturesand reduced nestling condition while maintaining their own condition.Overall, we found a strong individual quality effect: at thepopulation level, there was a trade-off between investing inincubation and maintaining parental condition, but among individuals,there was a positive correlation between change in parentalcondition and offspring quality. Individual differences in parentalstrategy can be important causes of life-history variation,especially through subtle, but important, aspects of reproductionsuch as maintaining egg temperature during incubation.     

Altitudinal and environmental variation in lifespan in the Copper butterfly Lycaena tityrus

1.  Variation in longevity within and between natural populations is widespread, and understanding the relative importance of environmental and genetic factors as well as their interactions in mediating such variation is crucial in longevity research.
2.  In this study lifespan of adult copper butterflies was examined in relation to altitude, temperature (20 and 27 °C), sex and adult feeding.
3.  As expected, longevity increased with decreasing temperature, and sucrose-fed butterflies had longer lifespans compared to water-fed and finally non-fed individuals. The impact of feeding, especially of having access to water or not, was larger at the higher compared to the lower temperature.
4.  Regarding altitudinal patterns, increased lifespan in high-altitude populations was largely restricted to beneficial feeding conditions, while under carbohydrate deprivation low-altitude animals lived longer, suggesting that low-altitude butterflies do better under food stress.
5.  Differences in longevity between sexes were small at 20 °C, while females lived substantially longer than males at the higher temperature. Consequently, females may be less susceptible to high temperature stress than males. Further, males suffered more from food stress than females, suggesting that females are generally more stress resistant than males.
6.  Using a full factorial design, this study demonstrates that variation in longevity is caused by several factors, and additionally by substantial interactive effects. Consequently, patterns of variation in longevity are complex, and one needs to be cautious when neglecting this source of variation, by focussing on individual factors only.     

Sex-specific variability in the immune system across life-history stages

Organisms theoretically manage their immune systems optimally across their life spans to maximize fitness. However, we lack information on (1) how the immune system is managed across life-history stages, (2) whether the sexes manage immunity differentially, and (3) whether immunity is repeatable within an individual. We present a within-individual, repeated-measures experiment examining life-history stage variation in the inflammatory immune response in the zebra finch (Taeniopygia guttata). In juveniles, age-dependent variation in immune response differed in a sex- and context-specific manner, resulting in no repeatability across stages. In adults, females displayed little stage-dependent variation in immune response when laying while receiving a high-quality (HQ) diet; however, laying while receiving a low-quality (LQ) diet significantly reduced both immune responses and reproductive outputs in a manner consistent with a facultative (resource-driven) effect of reproduction on immunity. Moreover, a reduced immune response in females who were raising offspring while receiving an HQ diet suggests a residual effect of the energetic costs of reproduction. Conversely, adult males displayed no variation in immune responses across stages, with high repeatability from the nonbreeding stage to the egg-laying stage, regardless of diet quality (HQ diet, r = 0.51; LQ diet, r = 0.42). Females displayed high repeatability when laying while receiving the HQ diet (r = 0.53); however, repeatability disappeared when individuals received the LQ diet. High-response females receiving the HQ diet had greater immune flexibility than did low-response females who were laying while receiving the LQ diet. Data are consistent with immunity being a highly plastic trait that is sex-specifically modulated in a context-dependent manner and suggest that immunity at one stage may provide limited information about immunity at future stages.     

Community structure of arboreal caterpillars within and among four tree species of the eastern deciduous forest

Abstract.  1. A seasonally replicated experimental design was used to address the question of how differences within and among host tree species affect arboreal caterpillar communities.
2. Seasonal variation influenced caterpillar community composition most significantly, and the similarity among caterpillar assemblages did not necessarily follow the pattern of phylogenetic relatedness among host trees.
3. Species richness and abundance of caterpillars were higher on oaks and maples than on American beech. Diversity partitioning models revealed that β diversity was only occasionally greater or less than expected by chance alone.
4. When β diversity was significant, values tended to be greater than expected by chance among replicate trees within each species and lower than expected by chance among the four tree species.
5. Differences among trees appeared important for determining patterns of species presence/absence for rare species and influencing patterns of species dominance within caterpillar assemblages. Differences among tree species had a significant effect on overall lepidopteran community composition and mean species diversity (i.e. α diversity).
6. Because β diversity of caterpillars among host trees was lower than expected by chance, host specificity within the Lepidoptera may be less prevalent than thought previously.     

Seasonal trade-offs in cell-mediated immunosenescence in ruffs (Philomachus pugnax)

The immune system is an energetically expensive self-maintenance complex that, given the risks of parasitism, cannot be carelessly compromised. Life-history theory posits that trade-offs between fitness components, such as self-maintenance and reproduction, vary between genders and age classes depending on their expected residual lifetime reproductive success, and seasonally as energetic requirements change. Using ruff (Philomachus pugnax), a bird with two genetically distinct male morphs, we demonstrate here a decrease in male immunocompetence during the breeding season, greater variance in immune response among males than females, immunosenescence in both sexes and male morphs, and a seasonal shift in the age range required to detect senescence. Using a phytohaemagglutinin delayed hypersensitivity assay, we assessed cell-mediated immunity (CMI) of males of typical breeding age during the breeding and nonbreeding seasons, and of a larger sample that included females and birds of a greater age range during the non-breeding period. CMI was higher for breeding-aged males in May than in November, but the increase was not related to age or male morph. In November, mean CMI did not differ between the sexes, but the variance was higher for males than for females, and there were no differences in mean or variance between the two male morphs. For both sexes and male morphs, CMI was lower for young birds than for birds of typical breeding ages, and it declined again for older birds. In males, senescence was detected in the non-breeding season only when very old birds were included. These results, generally consistent with expectations from life-history theory, indicate that the immune system can be involved in multifarious trade-offs within a yearly cycle and along an individual's lifetime, and that specific predictions about means and variances in immune response should be considered in future immunoecological research.     

Sex-specific variation in the emphasis,inducibility and timing of the post-mating immune response in Drosophila melanogaster

Ecological immunology attempts to explain variation in immune function. Much of this work makes predictions about how potential hosts should invest in overall immunity. However, this ‘overall’ perspective under-emphasizes other critical aspects, such as the specificity, inducibility and timing of an immune response. Here, we investigate these aspects by examining gene regulation across several immune system components in both male and female Drosophila melanogaster prior to and after mating. To elucidate potentially important temporal dynamics, we also assayed several genes over time. We found that males and females emphasized different components of their immune system, however overall investment was similar. Specifically, the sexes emphasized different gene paralogues within major gene families, and males tended to invest more in gram-negative defence. By contrast, the inducibility of the immune response was both transient (lasting approx. 24 hours) and equal between the sexes. Furthermore, mating tended to induce humoral gene upregulation, while cell-mediated genes were unaffected. Within the humoral system, gram-negative bacterial defence genes exhibited a greater inducibility than those associated with fungal or gram-positive bacterial defence. Our results suggest that variation in the effectiveness of the immune response between the sexes may be driven by differences in emphasis rather than overall investment.     

The ability to mount multiple immune responses simultaneously varies across the range of the tree swallow

Variation in immune responses is an important part of life history variation. When correlations between multiple immune measures are reported, studies report different patterns. I tested whether the correlation between levels of immune response was consistent across a species range. The ability of tree swallows Tachycineta bicolor to simultaneously produce immune responses to both a humoral immune response and T-cell mediated local inflammation to PHA was tested at three sites that span the breeding range. Females in Tennessee maintained stronger PHA responses than did females in either New York or Alaska. In New York and Alaska, individuals that produced strong PHA responses produced low levels of antibodies to a humoral challenge of sheep red blood cells (SRBC). However, in Tennessee, individuals that showed strong local PHA inflammation also mounted strong responses to SRBC. Increasing daily daytime temperatures led to increased PHA response, but there were no differences in the effect of temperature among sites. These results indicate spatial and/or temporal variation occurs in the ability to produce multiple immune responses simultaneously; this pattern suggests important geographic (or temporal) differences in factors driving investment in immune activity. In addition, these results suggest that studies extrapolating results across populations should be careful to consider geographic variation in immune activity.     

Seasonality determines patterns of growth and age structure over a geographic gradient in an ectothermic vertebrate

Environmental variation connected with seasonality is likely to affect the evolution of life-history strategies in ectotherms, but there is no consensus as to how important life-history traits like body size are influenced by environmental variation along seasonal gradients. We compared adult body size, skeletal growth, mean age, age at first reproduction and longevity among 11 common frog (Rana temporaria) populations sampled along a 1,600-km-long latitudinal gradient across Scandinavia. Mean age, age at first reproduction and longevity increased linearly with decreasing growth season length. Lifetime activity (i.e. the estimated number of active days during life-time) was highest at mid-latitudes and females had on average more active days throughout their lives than males. Variation in body size was due to differences in lifetime activity among populations??individuals (especially females) were largest where they had the longest cumulative activity period??as well as to differences between populations in skeletal growth rate as determined by skeletochronological analyses. Especially, males grew faster at intermediate latitudes. While life-history trait variation was strongly associated with latitude, the direction and shape of these relationships were sex- and trait-specific. These context-dependent relationships may be the result of life-history trade-offs enforced by differences in future reproductive opportunities and time constraints among the populations. Thus, seasonality appears to be an important environmental factor shaping life-history trait variation in common frogs.