Host-associated fitness variation in a seed beetle (Coleoptera: Bruchidae): evidence for local adaptation to a poor quality host

The geographic distributions of many generalist herbivores differ from those of their host plants, such that they experience coarse-grained spatial variation in natural selection on characters influencing adaptation to host plants. Thus, populations differing in host use are expected to differ in their ability to survive and grow on these host plants. We examine host-associated variation in larval performance (survivorship, development time, and adult body weight) and oviposition preference, within and between two populations ofStator limbatus (Coleoptera: Bruchidae) that differ in the hosts available to them in nature. In one population,Acacia greggii (Fabaceae: Mimosoideae) andCercidium microphyllum (Fabaceae: Caesalpininoideae) are each abundant, while in the second population onlyC. floridum andC. microphyllum are present. In both populations, egg-to-adult survivorship was less than 50% onC. floridum, while survivorship was greater than 90% onA. greggii. Most of the mortality onC. floridum occurred as larvae were burrowing through the seed coat; very low mortality occurred during penetration of the seed coat ofA. greggii. Significant variation was present between populations, and among families (within populations), in survivorship and egg-to-adult development time onC. floridum; beetles restricted toCercidium in nature, without access toC. floridum, survived better and developed faster onC. floridum than beetles that had access toA. greggii. Large host effects on body size were detected for female offspring: females reared onA. greggii were larger than those reared onC. floridum, whereas male offspring wee approximately the same size regardless of rearing host. Trade-offs between performance onC. floridum andC. floridum were not detected in this experiment. Instead, our data indicate that development time and survivorship onC. floridum may be largely independent of development time and survivorship onA. greggii. Patterns of oviposition preference corresponded to the observed patterns of host suitability: in laboratory preference tests, beetles with access toA. greggii in nature tended to prefer this host more than beetles without access to this host in nature.     

Egg components, egg size, and hatchling size in leatherback turtles

Relationships between egg size, egg components, and neonate size have been investigated across a wide range of oviparous taxa. Differences in egg traits among taxa reflect not only phylogenetic differences, but also interactions between biotic (i.e., maternal resource allocation) and abiotic (i.e. nest environment conditions) factors. We examined relationships between egg mass, egg composition, and hatchling size in leatherback turtles (Dermochelys coriacea) because of the unique egg and reproductive characteristics of this species and of sea turtles in general. Albumen comprised 63.0%+/-2.8% (mean+/-S.D.) of egg mass and explained most of the variation in egg mass, whereas yolk comprised only 33.0%+/-2.7%. Additionally, leatherback albumen dry mass was approximately 16% of albumen wet mass. Whereas hatchling mass increased significantly with egg mass (n = 218 clutches), hatchling mass increased by only approximately 2 g for each 10 g increase in egg mass and was approximately 10-20 g greater than yolk mass. Taken together, our results indicate that albumen might play a particularly significant role in leatherback embryonic development, and that leatherback eggs are both capable of water uptake from the nest substrate and also possess a large reservoir of water in the albumen. Relationships between egg mass and egg components, such as variation in egg mass being largely explained by variation in albumen mass and egg mass containing a relatively high proportion of albumen solids, are more similar to bird eggs than to eggs of other non-avian reptiles. However, hatchling mass correlates more with yolk mass than with albumen mass, unlike patterns observed in bird eggs of similar composition.     

Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments

Abstract In many organisms, large offspring have improved fitness over small offspring, and thus their size is under strong selection. However, due to a trade-off between offspring size and number, females producing larger offspring necessarily must produce fewer unless the total amount of reproductive effort is unlimited. Because differential gene expression among environments may affect genetic covariances among traits, it is important to consider environmental effects on the genetic relationships among traits. We compared the genetic relationships among egg size, lifetime fecundity, and female adult body mass (a trait linked to reproductive effort) in the seed beetle, Stator limbatus , between two environments (host-plant species Acacia greggii and Cercidium floridum ). Genetic correlations among these traits were estimated through half-sib analysis, followed with artificial selection on egg size to observe the correlated responses of lifetime fecundity and female body mass. We found that the magnitude of the genetic trade-off between egg size and lifetime fecundity differed between environments–a strong trade-off was estimated when females laid eggs on C. floridum seeds, yet this trade-off was weak when females laid eggs on A. greggii seeds. Also differing between environments was the genetic correlation between egg size and female body mass–these traits were positively genetically correlated for egg size on A. greggii seeds, yet uncorrelated on C. floridum seeds. On A. greggii seeds, the evolution of egg size and traits linked to reproductive effort (such as female body mass) are not independent from each other as commonly assumed in life-history theory.     

Population differences in host use by a seed-beetle: local adaptation, phenotypic plasticity and maternal effects

For insects that develop inside discrete hosts, both host size and host quality constrain offspring growth, influencing the evolution of body size and life history traits. Using a two-generation common garden experiment, we quantified the contribution of maternal and rearing hosts to differences in growth and life history traits between populations of the seed-feeding beetle Stator limbatus that use a large-seeded host, Acacia greggii, and a small-seeded host, Pseudosamanea guachapele. Populations differed genetically for all traits when beetles were raised in a common garden. Contrary to expectations from the local adaptation hypothesis, beetles from all populations were larger, developed faster and had higher survivorship when reared on seeds of A. greggii (the larger host), irrespective of their native host. We observed two host plant-mediated maternal effects: offspring matured sooner, regardless of their rearing host, when their mothers were reared on P. guachapele (this was not caused by an effect of rearing host on egg size), and females laid larger eggs on P. guachapele. This is the first study to document plasticity by S. limbatus in response to P. guachapele, suggesting that plasticity is an ancestral trait in S. limbatus that likely plays an important role in diet expansion. Although differences between populations in growth and life history traits are likely adaptations to their host plants, host-associated maternal effects, partly mediated by maternal egg size plasticity, influence growth and life history traits and likely play an important role in the evolution of the breadth of S. limbatus’ diet. More generally, phenotypic plasticity mediates the fitness consequences of using novel hosts, likely facilitating colonization of new hosts, but also buffering herbivores from selection post-colonization. Plasticity in response to novel versus normal hosts varied among our study populations such that disentangling the historical role of plasticity in mediating diet evolution requires the consideration of evolutionary history.     

Annual variation in the seasonal shift in egg size and clutch size in Sceloporus woodi

Summary Early and late season clutch parameters were examined over a three year period in the Florida scrub lizard, Sceloporus woodi. Precipitation levels were monitored throughout the study. In the early and late season of 1984 and the early season of 1986 precipitation levels approximated long-term mean levels of precipitation. In 1985 a severe winter drought occurred. Clutch size was positively related to body size in all samples in every year. In 1984 and 1986, egg size was not related to clutch size, whereas, in 1985 egg size was negatively related to clutch size. In 1985, females produced large clutches of small eggs early in the season and small clutches of large eggs late in the season. In 1984, no seasonal changes in egg or clutch size occurred. In the late season of 1986, females produced the largest clutches and the smallest eggs of all the samples, but egg and clutch size were not statistically different from the early season egg and clutch size of 1986. Total clutch dry weight, an estimate of total clutch energy, was not different in any of the six sampling periods. These data do not support current adaptationist models that attempt to explain the control of clutch and egg size in lizards. It is argued in this paper that egg and clutch size may vary in response to past environments that affect a female's physical condition, as well as, current resources that may be important for maintenance and reproduction. Egg and clutch size appear to be plastic traits selected to respond to proximal environmental variation, whereas, the investment of total dry matter/clutch has been optimized.     

Variation in inbreeding depression among populations of the seed beetle, Stator limbatus

Inbreeding depression has been documented in many insect species, but the degree to which it varies among traits within populations and among populations within species is poorly understood. We used a single‐generation factorial breeding design to examine variation in inbreeding depression among three populations of the seed‐feeding beetle, Stator limbatus Horn (Coleoptera: Chrysomelidae: Bruchinae), from the southwestern USA. Eggs from sib matings were less likely to develop and hatch, and larval hatch‐to‐adult mortality was higher for offspring of sib matings. Overall, inbreeding resulted in a reduction in the proportion of eggs that produced an adult from >80% for outbred matings in all three populations to an average of only 54% for inbred matings. Of those larvae that survived to adult, inbred beetles took ～1.5 days (>5%) longer to reach adult. The only measured trait not affected by inbreeding was adult body mass. The degree to which inbreeding increased mortality varied among the populations – inbreeding depression was lowest in the population that is most isolated. Although populations of S. limbatus are generally large in nature our results suggest that increased inbreeding associated with population fragmentation can have substantial effects on fitness of S. limbatus.     

The genetics and ecology of seed size variation in a biennial plant,Hydrophyllum appendiculatum (Hydrophyllaceae)

The goal of this study was to elucidate the sources of seed size variation in Hydrophyllum appendiculatum, an outcrossing, biennial plant. The genetic basis of seed size variation was examined with a diallel breeding design. The analysis did not reveal any evidence for additive genetic variance, suggesting that seed size could not evolve in response to natural selection. A series of greenhouse experiments was conducted to determine the sensitivity of seed weight to a number of ecological variables. Seed weight was affected by inbreeding depression: seeds produced by self-pollinations were significantly lighter that outcrossed seeds. Maternal plants did not differentially provision seeds that were the result of crosses between subpopulations (separated by 300 m) or between populations (separated by 1.7 km). Mean seed size was independent of the number of outcrossed pollen donors (one vs. many) that sired seeds on an inflorescence; however, the variance was greater on inflorescences pollinated by multiple donors. Direct manipulations of the abiotic environment showed that seed size was greater on plants growing under full sunlight compared to shaded plants. Seed size was unaffected by soil type, fertilizer addition, or defoliation. Finally, I determined the effect of varying pollination intensity at the level of a single inflorescence, and at the whole plant level. Seed weight was greatest on plants that had only 1 and 5 inflorescences pollinated, and least on those that had 10 and 20 pollinated. At the inflorescence level, seed weights were greatest on those where all flowers were pollinated, compared to inflorescences where only half of the flowers were pollinated. Perhaps the greatest contributor to variance in seed size in this species was the temporal decline within plants through the flowering season. These results indicate that maternal plants are not capable of producing uniform seed crops. Rather, the final distribution of seed size produced by plants within a population will necessarily vary and be the result of pollination effects, heterogeneity in the abiotic environment, and developmental constraints.     

Manipulation of parasitoid size using the temperature-size rule: fitness consequences

The phenotypic effects of rearing temperature on several fitness components of the koinobiont parasitoid, Aphidius colemani, were examined. Temperatures experienced during development induced a plastic linear response in the dry and fat masses of the immature stage and a non-linear response in the growth rate as well as in the size of adults. We investigated if the phenotypic morphometrical plasticity exhibited by parasitoids reared at different temperatures can induce variations in fitness-related traits in females. We did not find any difference in immature (pupal) mortality in accordance to rearing temperature. However, when examining adult longevity, we found an inverse linear relation with developmental temperature, confirming the usual rule that larger and fatter wasps live longer than smaller ones. The pattern of female fecundity was non-linear; wasps that developed at high and low temperatures were less productive. We suggest that when development is short, the accumulated reserves are not adequate to support both fecundity and survival. By manipulating adult size through changes in the rearing temperature, we showed that the usual shape of the size/fitness function is not always linear as expected. Developmental temperature induced a plasticity in energy reserves which affected the functional constraints between survival and reproduction.     

The effect of host size on quality attributes of the egg parasitoid,Trichogramma pretiosum

In a study of the quality ofTrichogramma pretiosum Riley (Hymenoptera: Trichogrammidae), we compared female wasps emerging from natural hosts, parasitized in the laboratory or the field with those emerging from factitious hosts used for commercial mass production. Females from the natural hosts were larger, more fecund, and longer lived than those from the factitious hosts. Compared to small females, large female wasps are substantially more fecund when honey (carbohydrate) is available but marginally more fecund when honey is unavailable. The size of a femaleT. pretiosum depends on two factors: the size of the host egg from which it emerges even when the wasp was gregarious, and the number of conspecifics that emerge with it. The similarities in the size distribution of female wasps emerging from natural hosts, in conjunction with the mechanism by whichTrichogramma measure host size and allocate eggs accordingly, suggests the hypothesis that size related components of fitness in femaleT. pretiosum are under strong selection in the field.     

Seasonal variation of egg size and number in a Daphnia pulex population

Seasonal variation of egg size and number was examined in a Daphnia pulex population inhabiting a vernal pond. In this population, size at maturity declines at midseason, probably as an adaptive response to size-selective predation by larvae of the salamander Ambystoma. The larger early season individuals produce more and larger eggs than the smaller late season individuals. Age at maturity does not vary between seasons. Laboratory experiments indicate that temperature may affect egg size, egg number and size at maturity. However, field data suggest that temperature accounts for only a small fraction of the total variation in egg size and number. Indirect measures of nutrition indicate that food limitation does not cause the seasonal decline in egg size and number. The seasonal change in reproductive traits is well correlated with changes in invertebrate and vertebrate predation. Examination of predator feeding preferences and their impact on Daphnia mortality indicate that variation of reproductive traits is most likely a complex adaptation to changing predation regimes.     

Experimentally reducing clutch size reveals a fixed upper limit to egg size in snakes, evidence from the king ratsnake, Elaphe carinata

Snakes are free of the pelvic girdle's constraint on maximum offspring size, and therefore present an opportunity to investigate the upper limit to offspring size without the limit imposed by the pelvic girdle dimension. We used the king ratsnake (Elaphe carinata) as a model animal to examine whether follicle ablation may result in enlargement of egg size in snakes and, if so, whether there is a fixed upper limit to egg size. Females with small sized yolking follicles were assigned to three manipulated, one sham-manipulated and one control treatments in mid-May, and two, four or six yolking follicles in the manipulated females were then ablated. Females undergoing follicle ablation produced fewer, but larger as well as more elongated, eggs than control females primarily by increasing egg length. This finding suggests that follicle ablation may result in enlargement of egg size in E. carinata. Mean values for egg width remained almost unchanged across the five treatments, suggesting that egg width is more likely to be shaped by the morphological feature of the oviduct. Clutch mass dropped dramatically in four- and six-follicle ablated females. The function describing the relationship between size and number of eggs reveals that egg size increases with decreasing clutch size at an ever-decreasing rate, with the tangent slope of the function for the six-follicle ablation treatment being -0.04. According to the function describing instantaneous variation in tangent slope, the maximum value of tangent slope should converge towards zero. This result provides evidence that there is a fixed upper limit to egg size in E. carinata.     

Patterns and fitness consequences of intraclutch variation in egg provisioning in tropical Australian frogs

Intraclutch variation in offspring size should evolve when offspring encounter unpredictable environmental conditions. This form of bet-hedging should maximise the lifetime reproductive success of individuals that engage it. We documented the numbers of eggs and means and variances of yolk volume in 15 frog species that occur in tropical savanna woodland. We experimentally determined the effects of initial yolk volume on larval growth patterns in four species. Intraclutch variation in yolk volume occurred to some degree in all species surveyed. Some species had very low, others had very high, intraclutch variation in yolk volume, but all species in which some clutches were highly variable also produced clutches with low variability. Species that occur in areas where the offspring environment is likely to be unpredictable had elevated levels of intraclutch variation in egg provisioning. There was no trade-off between egg size and number in any species surveyed. Under benign laboratory conditions, tadpoles from eggs with larger yolk volumes hatched at larger sizes, and these size differences persisted through a substantial proportion of the larval stage. This indicates that intraclutch variation in egg size has major offspring and thus parental fitness consequences, and is therefore a functional selection variable. This study provides evidence in support of models which predict that intraclutch variation in offspring provisioning can evolve in organisms that reproduce in unpredictable habitats.     

Post-dispersal predation of Acacia farnesiana seeds by Stator vachelliae (Bruchidae) in Central America

Summary Post-dispersal seed predation by the bruchid beetle Stator vachelliae was investigated in Santa Rosa National Park, Costa Rica. This insect finds the seeds of the leguminous Acacia farnesiana in the feces of horses, deer, and ctenosaur lizards, the current major dispersers. Patterns of oviposition and pre-adult survival of beetles in the seeds were investigated in a series of experiments using fresh horse dung. S. vachelliae never minded into the dung balls, attacking only those seeds located on the surface. Fresh horse dung did not attract insects more readily than dry dung. The proportion of seeds attacked was not related to their density in a defecation, and was similar in three areas with different densities of the host plant. In a fourth area with no fruiting A. farnesiana shrubs all seeds survived insect predation. Bruchids attacked a greater proportion of seeds at 1 m than at 5 m from the edge of the shrub's crown. Seeds were mainly removed from horse dung by rodents with similar intensity in all areas and at both distances; this seed removal interfered with bruchid oviposition and probably with bruchid survival. S. vachelliae oviposited less frequently on seeds in dung fully exposed to sun. When oviposition on a dung pile was high, the distribution of eggs on the seeds was clumped, suggesting that some seeds were preferred to others. By the end of the dry season, bruchids stopped attacking the seeds. The results show that the fate of both seeds and bruchids is greatly influenced by the location and time of defecation.     

The relationship among egg size,density and food level on larval development in the wood frog (Rana sylvatica)

Summary Although inter- and intraspecific variation in egg size among amphibians has been well documented, the relationship between egg size and fitness remains unclear. Recent attempts to correlate egg size intraspecifically with larval developmental patterns have been equivocal. In this study the development of larvae derived from large eggs and small eggs, from a single population in Maryland were compared under a range of food levels and larval population densities. Both food level and density had significant effects on the length of the larval period and size at metamorphosis. However, the response among larvae derived from different egg sizes was not additive. At low densities and high food levels, larvae from small eggs had longer larval periods and a larger size at metamorphosis than larvae derived from large eggs. In contrast, at high densities larvae from small eggs had longer developmental periods but were smaller at metamorphosis than larvae from large eggs. In addition, larvae from small eggs were more sensitive to density irrespective of food level. These results suggest that optimal egg size is correlated with environmental factors, which may explain the maintenance of both geographic and within population variation in egg size commonly observed in amphibians.     

Temperature effects on egg size and their fitness consequences in the yellow dung fly Scathophaga stercoraria

Organisms and parts of an organism like eggs or individual cells developing in colder environments tend to grow bigger. A unifying explanation for this Bergmann's rule extended to ectotherms has not been found, and whether this is an adaptive response or a physiological constraint is debated. The dependence of egg and clutch size on the mother's temperature environment were investigated in the yellow dung fly Scathophaga stercoraria. Smaller eggs were laid at warmer temperatures in the field and the laboratory, where possible confounding variables were controlled for. As clutch size at the same time was unaffected by temperature, this effect was not due to a trade-off between egg size and number. Temperature-dependent egg sizes even persisted within individuals: when females were transferred to a cooler (warmer) environment, they laid third-clutch eggs that were larger (smaller) than their first-clutch eggs. The fitness consequences of these temperature-mediated egg sizes were further investigated in two laboratory experiments. Neither egg and pre-adult survivorship nor larval growth rate were maximized, nor was development time minimized, at the ambient temperature corresponding to the mother's temperature environment. This does not support the beneficial acclimation hypothesis. Instead, this study yielded some, but by no means conclusive indications of best performance by offspring from eggs laid at intermediate temperatures, weakly supporting the optimal temperature hypothesis. In one experiment the smaller eggs laid at 24 °C had reduced survivorship at all ambient temperatures tested. Smaller eggs thus generally performed poorly. The most parsimonious interpretation of these results is that temperature-mediated variation in egg size is a maternal physiological response (perhaps even a constraint) of unclear adaptive value. This revised version was published online in November 2006 with corrections to the Cover Date.     

Individual variation in two host plants of the ladybird beetle,Epilachna pustulosa (Coleoptera: Coccinellidae)

Individual variation in two species of host plants (thistle,Cirsium kamtschaticum, and blue cohosh,Caulophyllum robustum) of the herbivorous ladybird beetleEpilachna pustulosa was examined under laboratory conditions for their acceptability to adult beetles as a food resource, for adult preference and for larval performance. When clones of these plants were subjected to non-choice tests using posthibernating female beetles, there was found to be significant intraspecific variation among clones in terms of their acceptability, but interspecific variation was not detected. Significant intraspecific as well as interspecific variation were frequently detected in the two host plants when clones of these plants were subjected to choice tests using posthibernating female beetles; the magnitude of interspecific plant variation for beetle preference is not necessarily larger than that of intraspecific plant variation. Individual variation across plant species with respect to beetle larval performance was also significant. A positive correlation between adult preference and larval performance is suggested across the two taxonomically remote host plant species, thistle and blue cohosh, although this needs further investigation.     

Manipulation of laying effort reveals habitat-specific variation in egg production constraints in Great Tits (Parus major)

It has been suggested that a bird's clutch size is not limited by the amount of resources available at the time of laying but that differences in the availability of food for nestlings is the ultimate underlying factor determining spatio-temporal variations in clutch size. However, habitat-related variations in egg production ability has yet to be investigated explicitly. We studied the breeding of Great Tits Parus major in deciduous and coniferous forests in the same area. The sizes of both the clutches and the eggs were, on average, larger in the former habitat than in the latter. A number of females were induced to lay more eggs than usual by removing four eggs from designated experimental clutches early in the laying period. These manipulated females laid approximately one egg more than control females, with the number of additional eggs laid not differing between the habitats. However, in both study years the relative size of the extra eggs – relative to the mean size of earlier laid eggs of the same clutch – was smaller in the coniferous habitat than in the deciduous habitat, while there was no habitat-related difference in the relative size of the last-laid eggs of control clutches. This result indicates that some form of proximate limitation during egg-laying period can contribute to the relatively small clutches and eggs in the coniferous habitat. Our results emphasize the need to take egg production costs into account when attempting to account for spatial variation in the reproductive behaviour of birds.     

Egg size variation between the fluvial-lacustrine and lacustrine types of a landlocked <Emphasis Type="Italic">Rhinogobius</Emphasis> goby in the Lake Biwa water system

The egg size of a landlocked goby, Rhinogobius sp. (the orange form), in the Lake Biwa water system was compared between the fluvial-lacustrine and lacustrine types. The former spawned larger eggs than the latter in the laboratory under the same environmental conditions of water temperature and current. This difference in egg size was also found in the field among six local populations from tributary rivers and lake shore. These results suggested that egg size is largely associated with the life history type that has experienced a different selection regimen, such as the risk of larval starvation, associated with their respective life cycles.     

Colony size affects collective decision-making in the ant Temnothorax albipennis

Social insects are well-known for their ability to achieve robust collective behaviours even when individuals have limited information. It is often assumed that such behaviours rely on very large group sizes, but many insect colonies start out with only a few workers. Here we investigate the influence of colony size on collective decision-making in the house-hunting of the ant Temnothorax albipennis. In experiments where colony size was manipulated by splitting colonies, we show that worker number has an influence on the speed with which colonies discover new nest sites, but not on the time needed to make a decision (achieve a quorum threshold) or total emigration time. This occurred because split colonies adopted a lower quorum threshold, in fact they adopted the same threshold in proportion to their size as full-size colonies. This indicates that ants may be measuring relative quorum, i.e. population in the new nest relative to that of the old nest, rather than the absolute number. Experimentally reduced colonies also seemed to gain more from experience through repeated emigrations, as they could then reduce nest discovery times to those of larger colonies. In colonies of different sizes collected from the field, total emigration time was also not correlated with colony size. However, quorum threshold was not correlated with colony size, meaning that individuals in larger colonies adopted relatively lower quorum thresholds. Since this is a different result to that from size-manipulated colonies, it strongly suggests that the differences between natural small and large colonies were not caused by worker number alone. Individual ants may have adjusted their behaviour to their colony’s size, or other factors may correlate with colony size in the field. Our study thus shows the importance of experimentally manipulating colony size if the effect of worker number on the emergence of collective behaviour is to be studied. Received 13 December 2005; revised 9 May 2006; accepted 15 May 2006.