Proteins that are highly expressed and composed of amino acids that are costly to synthesize are likely to place a greater drain on an organism's energy resources than proteins that are composed of ingested amino acids or ones that are metabolically simple to produce. Silks are highly expressed proteins produced by all spiders and many insects. We compared the metabolic costs of silks spun by arthropods by calculating the amount of ATP required to produce their component amino acids. Although a definitive conclusion requires detailed information on the dietary pools of amino acids available to arthropods, on the basis of the central metabolic pathways, silks spun by herbivorous, Lepidoptera larvae require significantly less ATP to synthesize than the dragline silks spun by predatory spiders. While not enough data are available to draw a statistically based conclusion, comparison of homologous silks across ancestral and derived taxa of the Araneoidea seems to suggest an evolutionary trend towards reduced silk costs. However, comparison of the synthetic costs of dragline silks across all araneomorph spiders suggests a complicated evolutionary pattern that cannot be attributed to phylogenetic position alone. We propose that the diverse silk-producing systems of the araneoid spiders (including three types of protein glues and three types of silk fibroin), evolved through intra-organ competition and that taxon-specific differences in the composition of silks drawn from homologous glands may reflect limited or fluctuating amino acid availability. The different functional properties of spider silks may be a secondary result of selection acting on different polypeptide templates. (C) 1999 Elsevier Science B.V. All rights reserved.
If a mutualistic relationship entails providing services at a cost, selection will favor individuals that maximize the net benefits of the interaction and minimize the costs. Larvae of many species of lycaenid butterflies secrete nutritious food rewards to attending ants and, in return, receive protection against predators and parasitoids. Because ants typically recruit more workers to larger resources, by forming groups the larvae may ensure more reliable access to ants and thereby gain better protection. A further consequence of aggregating should be a change of the cost-benefit relationship for individual larvae. The larger the group, the smaller a single larva's influence will be on total ant density, which could lead to a smaller investment in secretion, thus reducing the per capita cost of cooperation. In this study, the influence of ant attendance, group size, and companion quality on larval investment was investigated. The interaction between the obligately ant-dependent lycaenid, Jalmenus evagoras, and its attendant Iridomyrmex ants was manipulated and the effect on larval secretion measured. As the level of ant attendance increased, the delivery of food rewards increased, both for solitary and for aggregated larvae. When aggregated, larvae provided less food rewards to ants than when solitary, and secretion rate decreased with increasing group size. Furthermore, larvae had lower secretion rates when paired with a bigger, more attractive larva than when paired with a smaller one. The considerable reduction in secretion rates for larvae in groups suggests that gaining protection at a lower secretion cost could be one factor that promotes aggregation in myrmecophilous lycaenids.
Exploring the factors governing the maintenance and breakdown of cooperation between mutualists is an intriguing and enduring problem for evolutionary ecology, and symbioses between ants and plants can provide useful experimental models for such studies. Hundreds of tropical plant species have evolved structures to house and feed ants, and these ant-plant symbioses have long been considered classic examples of mutualism. Here, we report that the primary ant symbiont, Allomerus cf. demerarae, of the most abundant ant-plant found in south-east Peru, Cordia nodosa Lam., castrates its host plant. Allomerus workers protect new leaves and their associated domatia from herbivory, but destroy flowers, reducing fruit production to zero in most host plants. Castrated plants occupied by Allomerus provide more domatia for their associated ants than plants occupied by three species of Azteca ants that do not castrate their hosts. Allomerus colonies in larger plants have higher fecundity. As a consequence, Allomerus appears to benefit from its castration behaviour, to the detriment of C. nodosa. The C. nodosa-ant system exhibits none of the retaliatory or filtering mechanisms shown to stabilize cheating in other cooperative systems, and appears to persist because some of the plants, albeit a small;minority, are inhabited by the three species of truly mutualistic Azteca ants.
The honeybee (Apis mellifera) visual system contains three classes of retinal photoreceptor cells that are maximally sensitive to light at 440 nm (blue), 350 nm (ultraviolet), and 540 nm (green), We performed a PCR-based screen to identify the genes encoding the Apis blue- and ultraviolet (UV)-sensitive opsins, We obtained cDNAs that encode proteins having a high degree of sequence and structural similarity to other invertebrate and vertebrate visual pigments. The Apis blue opsin cDNA encodes a protein of 377 amino acids that is most closely related to other invertebrate visual pigments that are thought to be blue-sensitive. The UV opsin cDNA encodes a protein of 371 amino acids that is most closely related to the UV-sensitive Drosophila Rh3 and Rh4 opsins. To test whether these novel Apis opsin genes encode functional visual pigments and to determine their spectral properties, we expressed them in the R1-6 photoreceptor cells of blind ninaE mutant Drosophila, which lack the major opsin of the fly compound eye. We found that the expression of either the Apis blue- or UV-sensitive opsin in transgenic flies rescued the visual defect of ninaE mutants, indicating that both genes encode functional visual pigments. Spectral sensitivity measurements of these flies demonstrated that the blue and UV visual pigments are maximally sensitive to light at 439 and 353 nm, respectively. These maxima are in excellent agreement with those determined previously by single-cell recordings from Apis photoreceptor cells and provide definitive evidence that the genes described here encode visual pigments having blue and UV sensitivity.
Rhodopsins (Rh), G-protein-coupled receptors with seven transmembrane (TM) helices, form the first step in visual transduction in most organisms. Although many long-wavelength (LW) vertebrate opsin sequences are known, less information is available for invertebrate LW sequences. By a combination of RT-PCR and cDNA library screening, we have cloned and sequenced the honeybee LW Rh gene. The deduced protein is composed of 378 amino acids (aa), appears to have seven TM regions, and contains many of the structures and key aa thought to be important for Rh function. Phylogenetic analysis of this sequence in relation to other invertebrate Rh reveals it to be a member of a new group of insect LW Rh.
Populations of the myrmecophilous lycaenid Falmenus evagoras Donovan were assessed for genetic structure at three hierarchical spatial scales: sites, geographically-defined subpopulations, and subpopulations defined by species of mutualistic ant-associate. Estimates of Wright's F-ST generated from multilocus electrophoretic data revealed low, though significant, amounts of genetic structure. Most structure was observed at the level of geographic subpopulations, suggesting that adult butterflies do not exhibit preferential mating and oviposition along the lines of ant associate. The genetic structure data, together with estimates of Nei's genetic distance (D) for pairwise site and subpopulation comparisons, suggest that F. evagoras populations are spatially and temporally dynamic. These patterns are considered in the context of extinction and recolonization models. The extreme patchiness of F. evagoras populations stems from the stringent requirements of both host plant and host ant, contributing to an extinction/ recolonization process. We discuss the key parameters influencing genetic cohesion versus differentiation under an extinction/recolonization regime, including mode of butterfly dispersal, site turnover rate, and the effects of host dispersal and phenology. This system provides a model of population-level consequences of certain mutualistic interactions as well as of a class of patterns arising from an extinction/recolonization process. (C) 1996 The Linnean Society of London
Abstract. Larvae of 17 Lycaenidae butterfly species from Europe, North America, South East Asia and Australia were observed to retain at least some of their adaptations related to myrmecophily even after parasitic braconid larvae have emerged from them. The myrmecophilous glandular organs and vibratory muscles of such larval carcasses remain functional for up to 8 days. The cuticle of lycaenid larvae contains extractable “adoption substances” which elicit antennal drumming in their tending ants. These adoption substances, as well, appear to persist in a functional state beyond parasitoid emergence, and the larval carcasses are hence tended much like healthy caterpillars. In all examples, the braconids may receive selective advantages through myrmecophily of their host larvae, instead of being suppressed by the ant guard. Interactions where parasitoids exploit the ant-mutualism of their lycaenid hosts have as yet been recorded only from the Apanteles group in the BraconidaeMicrogasterinae.
Moths and butterflies whose larvae do not feed on plants represent a decided minority slice of lepidopteran diversity, yet offer insights into the ecology and evolution of feeding habits. This paper summarizes the life histories of the known predatory and parasitic lepidopteran taxa, focusing in detail on current researchin the butterfly family Lycaenidae, a group disprotionately rich in aphytophagous feeders and myrmecophilous habits.
Laboratory experiments manipulating the diet of colonies of the facultatively polygynous ant, Leptothorax curvispinosus (Mayr), demonstrated that carbohydrates and protein have synergistic effects on egg numbers and brood production in colonies of this ant. Colonies receiving insect prey and sucrose grew significantly faster than colonies reared on unlimited supplies of either of these food types alone. This study also measured the effect of queen number on colony growth rates. Because the occurrence of multiple queens might affect colony growth only under certain nutritional conditions, polygynous colonies were reared in each of the three diet treatments. Queen number did not affect colony worker production in any of the three diet treatments; thus, individual queens in polygynous colonies produced far fewer workers per queen than did queens in monogynous colonies. There were no interaction effects between queen number and diet on colony growth. Several colonies which lacked morphologically distinct queens produced workers over the course of the experiment Using artificially established colonies of unmated workers, we found no evidence for parthenogenetic (thelytokous) reproduction in these colonies.
Certain aphid species produce sterile soldiers, morphologically and behaviorally specialized individuals that defend fertile colony members, some or all of which are clonemates. If the soldier morph is maintained by inclusive fitness advantages, its altruism should preferentially benefit relatives, suggesting a potential role for kin discrimination. We performed a field experiment on spatial segregation and two laboratory experiments on agonistic behavior among non-soldiers and by soldiers of the cerataphidine aphid, Ceratovacuna japonica. For the test of spatial segregation, we introduce a new method of nearest-neighbor analysis, by constructing a minimum spanning tree from the map of individual locations and comparing the numbers of within-group and between-group connections. The results provide no evidence of kin recognition abilities in this species. Members of different clones showed no tendency to segregate spatially, nor to direct displacement attempts against non-kin when competing for feeding sites. Soldiers were indiscriminately aggressive toward early instar reproductives from their own and other colonies. We discuss the implications of these findings for several evolutionary hypotheses on the maintenance of the soldier morph in aphids.
For several species of lepidoptera, most of the similar to 350-bp mitochondrial control-region sequences were determined. Six of these species are in one genus, Jalmenus; are closely related; and are believed to have undergone recent rapid speciation. Recent speciation was supported by the observation of low interspecific sequence divergence. Thus, no useful phylogeny could be constructed for the genus. Despite a surprising conservation of control-region length, there was little conservation of primary sequences either among the three lepidopteran genera or between lepidoptera and Drosophila. Analysis of secondary structure indicated only one possible feature in common-inferred stem loops with higher-than-random folding energies-although the positions of the structures in different species were unrelated to regions of primary sequence similarity. We suggest that the conserved, short length of control regions is related to the observed lack of heteroplasmy in lepidopteran mitochondrial genomes. In addition, determination of flanking sequences for one Jalmenus species indicated (i) only weak support for the available model of insect 12S rRNA structure and (ii) that tRNA translocation is a frequent event in the evolution of insect mitochondrial genomes.
Larvae and pupae of the Australian lycaenid butterfly, Jalmenus evagoras Donovan (Lepidoptera; Lycaenidae), are protected from parasites and predators by attendant ants. In return, the juveniles of J.evagoras secrete to the ants a solution containing substantial amounts of sugars and amino acids. Larvae of J.evagoras were reared from hatching until adult eclosion either with or without ants. Experiments were performed to examine whether fifth (final) instar larvae attempt to compensate for the nutrient loss to ants, by consuming more food, digesting food more efficiently, or extending development time. The presence or absence of ants had no effect on the feeding rate, efficiency of digestion or development time of fifth instar larvae. Larvae with ants converted a smaller proportion of ingested food into biomass, and consequently grew less than their counterparts without ants. Thus fifth instar larvae of J.evagoras do not appear to compensate for the nutrient loss to ants. Possible reasons for the failure to compensate are discussed.
1. Juveniles of the Australian lycaenid butterfly, Jalmenus evagoras (Donovan), secrete to ants a solution of sugars and amino acids, primarily serine. The attendant ants protect the larvae and pupae from parasites and predators.2. The effect of caterpillar nutrition on the defence provided by ants was investigated. Potted food plants of Acacia decurrens were either given water containing nitrogenous fertilizer or were given water alone. Fertilized plants had a higher nitrogen content than unfertilized plants.3. Fifth instar larvae of J.evagoras feeding on fertilized plants attracted a larger ant guard than those feeding on unfertilized plants. In the absence of caterpillars, ants were not differentially attracted to fertilized and unfertilized plants.4. In the presence of ants, over a 10-day period, larvae on fertilized plants survived better than larvae on unfertilized plants. In the absence of ants larvae survived equally on fertilized and unfertilized plants. It is concluded that larvae on fertilized plants attracted a larger ant guard, and thereby survived better, than larvae on unfertilized plants.5. Adult females of J.evagoras preferred to lay egg batches on fertiizedd rather than unfertilized plants, but they did not lay larger egg batches.