Asymmetry in structural defenses: insights into selective predation in the wild

Assessment of geographical patterns in fluctuating asymmetry (small, random differences between sides of bilateral characters) among populations shows promise as a tool to resolve the relative biomechanical importance of traits, in addition to being a possible indicator of habitat quality. We used 115 endemic freshwater populations of threespine stickleback (Gasterosteus aculeatus) from Haida Gwaii (Queen Charlotte Islands), British Columbia, Canada, to explore the degree of concordance between geographical variation of asymmetry in a predator defense structure (bony lateral plates) and geographical variation in several indirect measures of predation regime as well as several abiotic habitat variables. We found a geographical cline in the population frequency of lateral plate asymmetries, with reduced asymmetry in the southern clear-water regions of the archipelago characterized by long reaction distances and greater chance of capture by predators, and elevated asymmetry in the northern stained-water regions with poor visibility and low chances of capture. Lateral plate asymmetry was strongly correlated with expression of several defensive armor traits, including total plate numbers among populations, mean cross-sectional diameter of stickleback with the dorsal and pelvic spines erect, and mean degree of overlap between the plates and spine supports. There were no significant correlations between frequency of asymmetric fish and any of our abiotic habitat variables. Stickleback with structural plate asymmetries had fewer trout-induced scars than symmetric fish in the significant majority of populations, and there was a decrease in structural plate asymmetry with age in stained-water habitats, suggesting that trout predators may be selectively removing asymmetric fish in some lakes. This study provides evidence that geographical variation in developmental stability of threespine stickleback, as seen in the frequencies of asymmetry, reflects differences among populations in the importance of structural defenses to fitness rather than differences in habitat quality, and that asymmetry may be a target of selection by predators in wild populations.     

Modification of developmental instability and fitness: Malathion-resistance in the Australian sheep blowfly,Lucilia cuprina

The evolution of resistance to malathion byLucilia cuprina initially results in an increase in fluctuating asymmetry. Resistant flies are at a selective disadvantage, relative to susceptibles, in the absence of the insecticide. A fitness/asymmetry modifier of diazinon-resistant phenotypes ameliorates these effects resulting in malathion-resistant phenotypes of relative fitness and asymmetry similar to susceptibles. For the nine genotypic combinations of the modifier and malathion-resistance alleles, developmental time increases linearly with increasing asymmetry. Percentage egg hatch decreases linearly with increasing asymmetry. The initially disruptive effect of the malathion-resistant allele was partially dominant, the effect of the modifier dominant. The results are discussed in terms of developmental perturbation, asymmetry estimation and relative fitness to consider whether it is adequate to use changes in fluctuating asymmetry alone as measures of developmental instability. It is suggested that in some circumstances antisymmetry may indicate developmental instability and that the diazinon/malathion-resistance systems inL. cuprina may allow the relative importance of genetical and/or environmental developmental perturbations to be ascertained.     

Ectoparasites cause increased bilateral asymmetry of naturally selected traits in a colonial bird

Abstract Parasitism has been shown to correlate with levels of bilateral symmetry in some organisms, with more asymmetric individuals often having more parasites. However, few studies have shown experimentally that parasitism directly causes increased asymmetry. By fumigating some cliff swallow (Petrochelidon pyrrhonota) colonies and leaving others untreated, we investigated experimentally whether ectoparasitism by the cimicid swallow bug led to higher levels of asymmetry in length of wings, outer tail feathers, and tarsus among juvenile and adult birds. Juveniles from fumigated colonies measured soon after fledging had significantly less asymmetry in wing and outer tail length than juveniles from nonfumigated colonies; asymmetry in tarsus length was unaffected by parasitism. Adults that had undergone one or more post‐juvenal molts on the wintering grounds showed no differences in asymmetry between those reared in fumigated vs. nonfumigated colonies. These results show that ectoparasitism directly leads to increased feather asymmetry in cliff swallows, probably through parasite‐induced nutritional stress. Because wing and tail asymmetry impair flight performance and reduce foraging efficiency, the increased asymmetry caused by parasites represents a fitness cost to cliff swallows. This is among the few experimental studies to show an effect of parasites on asymmetry of naturally selected characters.     

Seasonal patterns of parasitism and differential susceptibility among species in macrolepidopteran assemblages on Salix nigra (Marsh) and Acer negundo L.

Abstract 1. Previous research has demonstrated that parasitism of larval macrolepidoptera on Acer negundo (box elder) is greater than that of larvae on Salix nigra. 2. In this study, percentage larval parasitism of species on box elder and black willow was calculated for distinct portions of the season, to determine if the higher levels of parasitism on box elder resulted from greater parasitism during a particular portion of the season. 3. Larval parasitism was higher on box elder regardless of the portion of the season; however, the seasonal pattern of parasitism differed for each tree species, i.e. late-season box elder parasitism increased and late-season black willow parasitism decreased relative to early- and mid-season parasitism. 4. The degree to which higher levels of parasitism were associated with host and parasitoid traits such as average larval abundance, number of species, type of host, and parasitoid species load of macrolepidoptera, as well as average number of species of parasitoids during each portion of the season was determined. 5. In addition, the possibility that differences in the pattern of parasitism on box elder and black willow were caused by the presence of a greater number of numerically dominant parasitoid species in late-season box elder was investigated. 6. None of the variables, other than type of host species, were associated with higher levels of parasitism in late-season box elder. 7. Late-season, single-tree species on box elder (i.e. species that occurred only on box elder) were more heavily parasitised, compared with dual-tree species. This difference was not observed earlier in the season nor on black willow. 8. Further, single-tree species on late-season box elder included three numerically dominant species that suffered significantly greater larval parasitism than any other type of species on either of the two trees. 9. This study supported previous predictions, that suggested the importance of larval coloration: there was a higher proportion of green larvae among the most highly parasitised host species, i.e. single-tree, numerically dominant species.     

Ecological fitness of a glyphosate-resistant Lolium rigidum population: Growth and seed production along a competition gradient

Repeated use of glyphosate has resulted in evolution of glyphosate-resistant Lolium rigidum populations in Australia. The relative growth, competitiveness and reproductive output of glyphosate resistant (R) and susceptible (S) L. rigidum phenotypes from a single population were compared in competition with wheat. Vegetative growth of R and S individuals was studied in response surface experiments in the glasshouse and seed production was measured using an additive neighbourhood design experiment conducted in pots outside during the normal growing season of L. rigidum in Australia. There were no significant differences in vegetative growth or competitiveness of the R and the S phenotypes. The mean weight of seeds produced by R plants was significantly greater than that produced by S individuals. In the absence of wheat and at low wheat densities, S plants produced more seeds than R plants. However, at higher crop densities, differences in seed production were not significant. This is the first study to compare components of fitness at key life history stages for glyphosate R and S phenotypes isolated from a single weed population. The results presented indicate important differences in resource allocation during the reproductive stage for R and S phenotypes. Subtle differences in life history strategies may be manipulated by agronomic management to exploit the potential ecological fitness costs of the R phenotype. Further studies are required to provide a greater understanding of the occurrence and extent of fitness costs associated with glyphosate resistance. This knowledge can then be incorporated into models that simulate resistance evolution to design management strategies to prevent and/or contain the spread of glyphosate resistance.     

Habitat dependent associations between parasitism and fluctuating asymmetry among endemic stickleback populations

Inconsistencies in the relationship between fluctuating asymmetry (FA) and fitness may be due to selection acting on the degree of trait asymmetry that differs among populations or among traits. We assessed relationships between parasite susceptibility and fluctuating asymmetry in the number of bony lateral plates among 83 populations of freshwater Gasterosteus aculeatus (three spined stickleback) and among lateral plate positions that vary in the selection they experience for symmetry. The correlation between FA and parasite infection was highly variable among samples. Excess of infected asymmetric G. aculeatus increased significantly as the robustness of structural predator defences decreased. This effect was found for one parasite species only (Eustrongylides sp.) and was slightly stronger in females. In addition, there was a trend for there to be an excess of infected females asymmetric in those lateral plates positions that did not experience selection for their symmetry, although the trend only approached significance. These results suggest that selection for trait symmetry can obscure relationships between fitness and individual-wide developmental stability, providing one possible explanation for some of the heterogeneity in FA/fitness relationships seen in the literature. These results are also consistent with previous reports showing that ecological segregation between symmetric and asymmetric G. aculeatus and between sexes can alter the FA/fitness relationship.     

Environmental and Genetic Effects on the Asymmetry Phenotype: Diazinon Resistance in the Australian Sheep Blowfly, Lucilia Cuprina

The asymmetry phenotype of diazinon-resistant flies lacking a fitness/asymmetry Modifier (+/+; R/-) was dominant and independent of developmental temperature, larval density and diazinon concentration. Asymmetry score, pooled over three bristle characters, was ~50% greater for these phenotypes than for those of modified genotypes (M/-; -/-) and unmodified susceptibles (+/+; S/S) reared under standard laboratory conditions. Modified and susceptible phenotypes showed increased asymmetry score for temperatures and larval densities above and below standard rearing conditions; a positive correlation was observed between diazinon concentration and asymmetry score. Single and multiple environmental stresses resulted in similar scores that approached, but never exceeded, those of unmodified resistant phenotypes. Irrespective of the developmental conditions anti-symmetry and fluctuating asymmetry were typically observed for each bristle character of unmodified resistant and the modified and susceptible phenotypes, respectively. Thus while similar asymmetry scores could arise from genetic or environmental effects, asymmetry pattern was genetically based. Population cage analyses at different temperatures and larval densities showed a negative association between mean asymmetry and relative fitness.     

Patterns of fluctuating asymmetry in the limbs of anurans

It has been hypothesized that fluctuating asymmetry (FA) may provide an indication of the functional importance of structures within an organism, with structures that more strongly impact fitness being more symmetric. Based on this idea, we predicted that for tetrapods in which the forelimbs and hindlimbs play an unequal role in locomotion, the less functionally important limb set should display higher levels of FA. We conducted a multispecies test of this hypothesis in anurans (frogs and toads), whose saltatory locomotor mode is powered by the hindlimbs. We also tested whether FA in the forelimbs, which play a more important role during landing, differed between families that differ in the degree of forelimb use in locomotion (Bufonidae vs. Ranidae). We calculated FA from the lengths of humeri and femora measured from disarticulated skeletal specimens of four anuran taxa (Bufonidae: Anaxyrus americanus, Rhinella marina; Ranidae: Lithobates catesbeianus, Lithobates clamitans). Our findings were consistent with the hypothesis that natural selection for increased locomotor performance may influence patterns of FA seen in vertebrate limbs, with all species displaying lower mean FA in the hindlimbs. More subtle functional roles between the forelimbs of bufonids and ranids, however, did not elicit different levels of FA.     

Effect of nitrogen fertilizer level on infestations of lepidopterous stemborers and yields of maize in Zanzibar

The effect of nitrogen levels of 0, 60, 120, and 250 kg/ha and insecticide treatment (Furadan) on population densities and parasitism of lepidopteran stemborers, and maize yields were studied in Zanzibar during 2004/05. Chilo partellus (Swinhoe) (Lepidoptera: Crambidae) dominated by 3-fold over Sesamia calamistis Hampson (Lepidoptera: Noctuidae) and 42 fold over Chilo orichalcociliellus Strand (Lepidoptera: Crambidae). Stemborer density per plant and parasitism by Cotesia flavipes (Cameron) (Hymenoptera: Braconidae) increased with nitrogen application level. Percentage of bored internodes per plant caused by stemborer decreased with N levels during the short rainy season. Pesticide application reduced densities of all stemborer species during the short rainy season, when infestations were high. Maize yield increased 2 to 8 times with N level, compared to the zero treatment, but the effect was less pronounced in the protected plots.     

Population dynamics of Bemisia tabaci (Homoptera: Aleyrodidae) parasitoids on cassava mosaic disease–resistant and susceptible varieties

Three field trials were conducted at Namulonge Agricultural and Animal Production Research Institute to investigate the population dynamics of Bemisia tabaci Gennadius and its associated aphelinid parasitoids in Uganda. Results showed that more whitefly occurred on the cassava mosaic disease-resistant variety, (Nase 4) compared to the susceptible variety, (Ebwanatereka). Two species of aphelinid parasitoids, Eretmocerus mundus Mercet and Encarsia sophia Girault and Dodd, were identified during the study. Overall percent parasitism did not differ significantly (P>0.05) between varieties in all the trials, but significant differences occurred at 13, 15 and 21 weeks after planting during late season (2000), 18 weeks after planting during early season (2001), and 8 weeks after planting during late season (2001). The trends in the build up in numbers of both parasitoids species and apparent parasitism were similar, differed significantly on certain dates. It was, however, noted that percent parasitism decreased with nymph number. The significance of this phenomenon on the potential use of these aphelinid parasitoids as biocontrol agents of the cassava whitefly is discussed.     

Effects of the parasitic botfly Philornis carinatus on nestling house wrens,Troglodytes aedon,in Costa Rica

I studied the life cycle of a botfly (Diptera: Muscidae: Philornis carinatus) and examined the effects of botfly ectoparasitism on nestling house wrens (Passeriformes: Troglodytidae: Troglodytes aedon) during three years in Costa Rica. At three study sites, I found that nestlings were relatively unaffected by botflies, in contrast to all other studies of birds infected with philornid botflies. At Monteverde, the main study site, infected chicks grew slightly slower and had slightly shorter tarsi and wing chords than uninfected chicks, but both groups fledged at similar weights. Since weight at fledging is the only growth character associated with post-fledging survivorship, botfly infections likely cost wrens little in terms of fitness. At all sites, fledging success did not differ between infected and uninfected nests. Botfly infections were more prevalent at two lower elevation sites than at the high elevation Monteverde side. Infection prevalence increased during the nesting season at all study sites, which suggests a botfly life cycle in which adult population levels increase during the wren breeding season and then decline during a dormant period when wrens are not nesting. Finally, botflies may attack chicks throughout the period before fledging, but there is no indication they locate nests before hatching. In sum, botfly parasitism on wrens appears to be benign, perhaps because the study sites are at the edge of the botfly's range or because wrens are not a preferred host.     

Individual asymmetry as a predictor of fitness in the bat Carollia perspicillata

The measurement of fitness in wild populations is a challenging task, and a number of proxies have been proposed with different degrees of success. Developmental instability/stability (DI) is an organismal property associated with variance in bilateral asymmetry (fluctuating asymmetry—FA) and a correlated effect on fitness. This study provides evidence to corroborate the hypothesis that asymmetry partly reflects DI and is correlated with a reduction in fitness measured by survival and reproduction in bats. We studied two colonies of the bat Carollia perspicillata in southeastern Brazil over 5 years, marking and recapturing individuals. Gaussian mixture models for signed Forearm Asymmetry (ForA) distribution indicated that ~20% of asymmetry variation was due to DI heterogeneity among individuals. ForA, body condition (Scaled Mass Index—SMI) and Forearm Length (ForL) were used as predictors of survival probability in Cormack‐Jolly‐Seber models. Asymmetry was negatively associated with survival, whereas SMI and ForL were positively associated. The male C. perspicillata defend sites within the roost that are favoured by female harems, but there are mating opportunities for bachelor males, leading to both territorial disputes and sperm competition. As predicted by sexual selection, ForA was negatively associated with relative Testicle Length, a measure of reproductive potential. In females, ForA was negatively associated with the probability of two pregnancies (as opposed to one) in a given breeding season. The effect magnitudes and directions of associations suggest that asymmetry, even though not perfectly reflecting DI variation, is a useful predictor for fitness components in C. perspicillata.     

Bad guys turned nice? A critical assessment of Wolbachia mutualisms in arthropod hosts

Wolbachia are the most abundant bacterial endosymbionts among arthropods. Although maternally inherited, they do not conform to the widespread view that vertical transmission inevitably selects for beneficial symbionts. Instead, Wolbachia are notorious for their reproductive parasitism which, although lowering host fitness, ensures their spread. However, even for reproductive parasites it can pay to enhance host fitness. Indeed, there is a recent upsurge of reports on Wolbachia‐associated fitness benefits. Therefore, the question arises how such instances of mutualism are related to the phenotypes of reproductive parasitism. Here, we review the evidence of Wolbachia mutualisms in arthropods, including both facultative and obligate relationships, and critically assess their biological relevance. Although many studies report anti‐pathogenic effects of Wolbachia, few actually prove these effects to be relevant to field conditions. We further show that Wolbachia frequently have beneficial and detrimental effects at the same time, and that reproductive manipulations and obligate mutualisms may share common mechanisms. These findings undermine the idea of a clear‐cut distinction between Wolbachia mutualism and parasitism. In general, both facultative and obligate mutualisms can have a strong, and sometimes unforeseen, impact on the ecology and evolution of Wolbachia and their arthropod hosts. Acknowledging this mutualistic potential might be the key to a better understanding of some unresolved issues in the study of Wolbachia–host interactions.     

Parasitism of the Wheat Stem Sawfly (Hymenoptera: Cephidae) in Montana

The wheat stem sawfly,Cephus cinctusNorton (Hymenoptera: Cephidae) was first found in wild grasses and soon became an economically important pest of wheat after cultivation began in the northern Great Plains. Of the species of parasitoids that attackC. cinctusin wild grasses, onlyBracon cephi(Gahan) andB. lissogasterMuesebeck (Hymenoptera: Braconidae) have been found in wheat. Levels of parasitism vary between wheat-producing regions in Montana. Parasitism levels were increased by releasing individuals from a region with high levels of parasitism into a region where parasitism levels were low. This suggests that there has been unequal rates of parasitoid adaptation from wild grasses to wheat in different regions of Montana.     

Sex-Specific Correlations of Individual Heterozygosity,Parasite Load,and Scalation Asymmetry in a Sexually Dichromatic Lizard

Heterozygosity-fitness correlations (HFCs) provide insights into the genetic bases of individual fitness variation in natural populations. However, despite decades of study, the biological significance of HFCs is still under debate. In this study, we investigated HFCs in a large population of the sexually dimorphic lizard Takydromus viridipunctatus (Lacertidae). Because of the high prevalence of parasitism from trombiculid mites in this lizard, we expect individual fitness (i.e., survival) to decrease with increasing parasite load. Furthermore, because morphological asymmetry is likely to influence individuals'' mobility (i.e., limb asymmetry) and male biting ability during copulation (i.e., head asymmetry) in this species, we also hypothesize that individual fitness should decrease with increasing morphological asymmetry. Although we did not formally test the relationship between morphological asymmetry and fitness in this lizard, we demonstrated that survival decreased with increasing parasite load using a capture-mark-recapture data set. We used a separate sample of 140 lizards to test the correlations between individual heterozygosity (i.e., standardized mean d² and HL based on 10 microsatellite loci) and the two fitness traits (i.e., parasite load and morphological asymmetry). We also evaluated and excluded the possibility that single-locus effects produced spurious HFCs. Our results suggest male-only, negative correlations between individual heterozygosity and parasite load and between individual heterozygosity and asymmetry, suggesting sex-specific, positive HFCs. Male T. viridipunctatus with higher heterozygosity tend to have lower parasite loads (i.e., higher survival) and lower asymmetry, providing a rare example of HFC in reptiles.     

Fluctuating asymmetry, call structure and the risk of attack from phonotactic parasitoids in the bushcricket Sciarasaga quadrata (Orthoptera: Tettigoniidae)

The acoustically orienting parasitoid Homotrixa alleni (Diptera: Tachinidae) is a significant mortality factor of calling male Sciarasaga quadrata (Orthoptera: Tettigoniidae), with less than 10% of males escaping parasitism within the duration of the calling season. This study examined fluctuating asymmetry (FA) (small, random deviations from perfect symmetry) in five morphological traits in S. quadrata and its relation to the survival of calling males in the field. A significant relationship was demonstrated in only a single trait; across three consecutive field seasons and among each of the collections per season, parasitised males were shown to have significantly more asymmetric hind tibia than unparasitised males. Since the morphological development of males is complete prior to parasitoid attack, this relationship is not caused by the activities of the parasitoid. Further experimentation revealed that there was no relationship between the level of FA in the hind tibia and the success of parasitism, with males artificially parasitised in the laboratory showing no difference in FA from those where parasitism was unsuccessful. Instead, FA was shown to be negatively related to chirp length, an aspect of call structure that significantly affects the survival of calling males under parasitism risk in the field. We explore the possible reasons why more asymmetric males produce calls of shorter chirp length and hypothesise that the difference in hind tibia asymmetry seen between parasitised and unparasitised males in the field is related to host location in H. alleni rather than the inability of S. quadrata to defend itself against parasitoid attack. Received: 14 November 1997 / Accepted: 20 April 1998     

<Emphasis Type="SmallCaps">P</Emphasis>lastic responses to temporal variation in moisture availability: consequences for water use efficiency and plant performance

The ability to appropriately modify physiological and morphological traits in response to temporal variation should increase fitness. We used recombinant hybrid plants generated by crossing taxa in the Piriqueta caroliniana complex to assess the effects of individual leaf traits and trait plasticities on growth in a temporally variable environment. Recombinant hybrids were used to provide a wide range of trait expression and to allow an assessment of the independent effects of individual traits across a range of genetic backgrounds. Hybrid genotypes were replicated through vegetative propagation and planted in common gardens at Archbold Biological Station in Venus, Florida, where they were monitored for growth, leaf morphological characters, and integrated water use efficiency (WUE) (C isotope ratio; δ¹³C) for two successive seasons. Under wet conditions only leaf area had significant effects on plant growth, but as conditions became drier, growth rates were greatest in plants with narrow leaves and higher trichome densities. Plants with higher WUE exhibited increased growth during the dry season but not during the wet season. WUE during the dry season was increased for plants with smaller, narrower leaves that had higher trichome densities and increased reflectance. Examination of alternative path models revealed that during the dry season leaf traits had significant effects on plant growth only through their direct effects on WUE, as estimated from δ¹³C. Over the entire growing season, plants with a greater ability to produce smaller and narrower leaves with higher trichome densities in response to reduced water availability had the greatest growth rate. These findings suggest that plants making appropriate changes to leaf morphology as conditions became dry had increased WUE, and that the ability to adjust leaf phenotypes in response to environmental variation is a mechanism by which plants increase fitness.     

Costs of reproduction in male lizards, Sceloporus virgatus

Models of life history evolution typically assume a balance between the benefits of current reproductive activity and the costs to future reproductive success or survivorship, but empirical studies often find positive correlations between such components of fitness in undisturbed animal populations. I examined possible survivorship costs of reproduction in free-ranging male lizards, Sceloporus virgatus , and found that males with low levels of mating success were less likely to survive to the following breeding season. I also investigated two possible indicators of reproductive effort, increase in ectoparasite load and decrease in body weight during the breeding season. Levels of parasitism with trombiculid mites at the end of the breeding season were not associated with any measure of fitness or body condition (mating success, survivorship to the following year, relative weight loss). Yearling males (which have low levels of mating success) usually gained weight during the breeding season, while older males generally lost weight during this period. This suggests that young males may have postponed reproduction in favor of body growth and that seasonal weight loss of older males might reflect reproductive effort. Within the group of older males, individuals with the highest levels of mating success did not have high levels of either weight loss or mortality. Mate guarding behavior, an alternative to the aggressive territorial behavior typical of many lizard species, may allow certain males to obtain mates without expending large amounts of energy or exposing themselves to great mortality risks.