High Fitness Cost Research Articles

Single Amino Acid Mutations in the Cadherin Receptor from Heliothis virescens Affect Its Toxin Binding Ability to Cry1A Toxins

Bacillus thuringiensis Cry protein exerts its toxic effect through a receptor-mediated process. Both aminopeptidases and cadherin proteins were identified as putative Cry1A receptors from Heliothis virescens and Manduca sexta. The importance of cadherin was implied by its correlation with a Cry1Ac resistant H. virescens strain (Gahan, L. J., Gould, F., and Heckel, D. G. (2001) Science 293, 857-860). In this study, the Cry1Ac toxin-binding region in H. virescens cadherin was mapped to a 40-amino-acid fragment, from amino acids 1422 to 1440. This site overlaps with a Cry1Ab toxin-binding site, amino acids 1363-1464 recently reported in M. sexta (Hua, G., Jurat-Fuentes, J. L., and Adang, M. J. (2004) J. Biol. Chem. 279, 28051-28056). Further, feeding of the anti-H. virescens cadherin antiserum or the partial cadherins, which contain the toxin-binding region, in combination with Cry1Ab/Cry1Ac reduced insect mortality by 25.5-55.6% to first instar H. virescens and M. sexta larvae, suggesting a critical function for this cadherin domain in insect toxicity. Mutations in this region, to which the Cry1Ac binds through its loop 3, resulted in the loss of toxin binding. For the first time, we show that the cadherin amino acids Leu(1425) and Phe(1429) are critical for Cry1Ac toxin interaction, and if substituted with charged amino acids, result in the loss of toxin binding, with a K(D) of < 10(-5) m. Mutation of Gln(1430) to an alanine, however, increased the Cry1Ac affinity 10-fold primarily due to an increase on rate. The L1425R mutant can result from a single nucleotide mutation, CTG --> CGG, suggesting that these mutants, which have decreased toxin binding, may lead to Cry1A resistance in insects.

COMPETITION, HERBIVORY, AND REPRODUCTION OF TRICHOME PHENOTYPES OF DATURA WRIGHTII

The trichome dimorphism of Datura wrightii is intriguing because glandular trichome production has a high fitness cost. Plants producing glandular trichomes (''sticky'' plants) are resistant to many insect herbivores that attack plants producing nonglandular trichomes (''velvety'' plants). When protected from herbivores, sticky plants initially pro- duce fewer seeds than velvety plants but grow to a larger size. In a three-year field ex- periment, we tested the hypothesis that sticky plants acquire a competitive advantage through greater vegetative growth. In the absence of herbivores, sticky and velvety plants grew to similar sizes in their first year, but sticky plants grew larger in the second and third years. Seed production of sticky plants was 46-60% less than velvety plants in their first year, and this caused a 13% reduction in their finite rate of increase overall, even though sticky plants produced more seeds than velvety plants did in later years. The impact of herbivory varied with plant density, and herbivores reduced plant fitness more at low plant density than at high plant density. The differences in growth associated with trichome morphology occurred too late to provide a competitive advantage to sticky plants and probably contribute little to the maintenance of D. wrightii's trichome dimorphism.

Age at first breeding and fitness in goshawk Accipiter gentilis

Summary Age at first breeding has a large influence on fitness and hence is crucial to the evolution of life‐history strategies. Goshawks Accipiter gentilis start breeding aged 1–4 years. Using 30 years of data and both lifetime reproductive success (LRS) and lind as a fitness estimate for 74 female goshawks, I showed that the optimal age at first reproduction was 3 years in this population. Females that started to breed earlier had lower LRS and lind, not because of reduced life span, but because of lower reproduction at early ages. The constraint hypothesis, which states that foraging or other skills improve with age was the most likely explanation for the higher reproduction with increasing age. Incorporating habitat heterogeneity provided the mechanism that explained not only the fitness cost to early maturity, but also why this cost was heterogeneous. Females starting to breed aged 1 suffered a very high fitness cost if they were in a bad‐quality territory, but fitness costs were small when they were in a good‐quality territory. This explains why I found evidence for a nonlinear selection pressure on age at first breeding. Population density also affected whether a female started to breed early or not: over the study period, population density increased and the percentage of females starting to breed aged 1 decreased. The optimal age at first breeding seems to be a trait affected by a complex interplay between cost and benefits of early reproduction mediated by habitat heterogeneity and population density.

The biology and behavior of the longhorned beetle, Dectes texanus on sunflower and soybean

The biology and behavior of the longhorned beetle Dectes texanus LeConte (Coleoptera: Cerambycidae) was studied on two host plants that suffer economic losses from this pest; sunflower, Helianthus annuus, and soybean, Glycines max. Reciprocal crosses of D. texanus collected from the two plants all produced viable progeny, indicating that conspecific insects attack both crops. Pupae from soybean stalks weighed about 40% less than those from sunflower, and adults fed on soybean lived a mean of 23 days, compared to a mean of 53 days (males) and 76 days (females) for those fed sunflower. A female's larval host plant had no effect on her tendency to ovipuncture plants of either type in a greenhouse trial. A field-tested population collected exclusively from sunflower contained three types of females in similar proportions: those that laid eggs only on sunflower, those that laid only on soybean, and those that laid equally on both host plants. Females in field trials fed more on the plant they had fed on in the laboratory, but soybean-fed females fed more on soybean than did sunflower-fed females. Females fed soybean also made more ovipunctures on soybean plants in field trials than sunflower-fed females, but their responses to sunflower plants were similar. Females displayed higher total ovipositional activity when they encountered sunflower first in the field, and lower total activity when they encountered soybean first. Feeding scores were significantly correlated with ovipunctures and eggs on both plant types. We conclude that sunflower is the preferred host plant, although females will accept soybean when it is the only available food. The results suggest that D. texanus is still in the initial stages of a host range expansion with female host selection behavior demonstrating both genetic influences and phenotypic flexibility. Sunflower represents a nutritionally superior, ancestral host plant and relatively high fitness costs are still associated with utilization of the novel host plant, soybean, costs that may be offset by benefits such as reduced intraspecific competition. These potential benefits and their consequent implications for D. texanus host range evolution are hypothesized and discussed.

Sympathetic and T helper (Th)2 bias may ameliorate uterine fibroids, independent of sex steroids

We propose that inadequate sympathetic bias and Th2 bias in the uterine environment contributes to the formation of fibroids, independent of the sex steroid status. We also propose that fibroids represent a modern maladaptation that partly results from decreasing exposure to seminal fluid, which contains catecholalmines, transforming growth factor beta1 (TGFbeta1), aldosterone, prostaglandins, and other factors that shift the uterine environment to sympathetic and T helper (Th)2 bias. Lower risk of fibroids is associated with pre-menarche, post-menopause, pregnancy, exposure to contraceptives, smoking, earlier age of first pregnancy, shorter interval since last pregnancy, higher parity, and non-obesity. These associations are currently attributed to alterations of sex steroids. However, the association may also be explained by the observation that pre-menarche, post-menopause, pregnancy, and smoking represent periods of sympathetic and Th2 bias. Furthermore, use of contraceptives, early age of first pregnancy, short interval since last pregnancy, high parity, abnormal pap smear, and non-obesity may represent surrogates for increased sexual activity and increased exposure to seminal fluid. Catecholalmines, aldosterone, TGF, and prostaglandins are among the seminal fluid components that promote sympathetic and Th2 bias. Vasectomized copulations protect against fibroids, an observation that undermines the steroid hypothesis and supports our hypothesis. The putative mechanism of action of uterine artery embolization (UAE) for fibroid treatment is starvation of blood supply, but the extensive collaterals that protect uterine perfusion would presumably also buffer against fibroid hypoperfusion. Instead, the sympathetic and Th2 responses to UAE-related ischemia may contribute to fibroid regression. A potential explanation for the association of fibroids with intrauterine devices may be a Th1 cell-mediated immune response to the foreign body, which may also enhance the contraceptive effect. Novel methods of preventing and treating fibroids by promoting sympathetic and Th2 shift through natural, pharmacologic, and neuromodulatory means are envisioned. Fibroids are likely a modern dysfunction given the high Darwinian fitness cost of fibroid-related infertility, and may be attributable to reduced intercourse frequency. Fibroids have been observed among animals in captivity that are presumably reproductively isolated.

Transient masculinization in the fossa, Cryptoprocta ferox (Carnivora, Viverridae).

In at least 9 mammalian species, females are masculinized throughout life, but the benefits of this remain unclear despite decades of thorough study, in particular of the spotted hyaena (Crocuta crocuta) in which the phenomenon has been associated with a high fitness cost. Through examination of wild and captive fossas (Cryptoprocta ferox, Viverridae), androgen assays, and DNA typing for confirmation of gender, we made the first discovery of transient masculinization of a female mammal. Juvenile female fossas exhibited an enlarged, spinescent clitoris supported by an os clitoridis and a pigmented secretion on the underpart fur that in adults was confined to males. These features appeared to diminish with age. The majority of adult females lacked them, and os clitoridis length was inversely related to head-body length. No evidence was found to link this masculinization to elevated female androgen levels. Circulating concentrations of testosterone and androstenedione, but not dihydrotestosterone, were significantly lower in females than in males. No significant differences in testosterone, androstenedione, or dihydrotestosterone levels were found between juvenile (masculinized) and adult (nonmasculinized) females. There are several possible physiological mechanisms for this masculinization. None of the hypotheses so far proposed to explain the evolutionary basis of female masculinization in mammals are applicable to our findings. We present 2 new hypotheses for testing and development.

Dissecting the cost of insecticide resistance genes during the overwintering period of the mosquito Culex pipiens.

In several insects, there appears to be a high fitness cost associated with insecticide resistance genes during the overwintering period. In order to understand when and how this cost operates, all mosquitoes entering a natural cave for overwintering were regularly sampled, and their resistance genes at two loci (Ester and Ace.1) were individually identified. During the main period of entry (October and November), susceptible mosquitoes were first observed, followed by resistant ones, this trend being similar for both loci. This observation is best explained by a migration phenomenon, northern and more susceptible populations starting to overwinter first, followed by southern and more resistant ones. During the remaining part of the winter (December-March), mosquitoes entering the cave were still caught and they probably corresponded to individuals leaving a former overwintering site in search of a more suitable one. A lower overall frequency of resistant phenotypes was found in the second part of the winter at Ester, suggesting that a large fitness cost (42%) had operated. A decreasing frequency of resistant phenotypes was also found at Ace.1, indicating a large survival cost of resistant mosquitoes (7% for the homozygote Ace.1R) in their former overwintering site. These results are discussed in the light of the local evolution of these resistance genes in southern France.

Estimates of the Rate and Distribution of Fitness Effects of Spontaneous Mutation in Saccharomyces cerevisiae

The per-genome, per-generation rate of spontaneous mutation affecting fitness (U) and the mean fitness cost per mutation (s) are important parameters in evolutionary genetics, but have been estimated for few species. We estimated U and sh (the heterozygous effect of mutations) for two diploid yeast strains differing only in the DNA mismatch-repair deficiency used to elevate the mutation rate in one (mutator) strain. Mutations were allowed to accumulate in 50 replicate lines of each strain, during 36 transfers of randomly chosen single colonies (approximately 600 generations). Among wild-type lines, fitnesses were bimodal, with one mode showing no change in mean fitness. The other mode showed a mean 29.6% fitness decline and the petite phenotype, usually caused by partial deletion of the mitochondrial genome. Excluding petites, maximum-likelihood estimates adjusted for the effect of selection were U = 9.5 x 10(-5) and sh = 0.217 for the wild type. Among the mutator lines, the best fit was obtained with 0.005 < or = U < or = 0.94 and 0.049 > or = sh > or = 0.0003. Like other recently tested model organisms, wild-type yeast have low mutation rates, with high mean fitness costs per mutation. Inactivation of mismatch repair increases the frequency of slightly deleterious mutations by approximately two orders of magnitude.

DOES TESTOSTERONE AFFECT THE TRADE-OFF BETWEEN INVESTMENT IN SEXUAL/TERRITORIAL BEHAVIOUR AND PARENTAL CARE IN MALE GREAT TITS?

Abstract Breeding testosterone (T) profiles of free-living male birds are hypothesized to reflect a trade-off between investment in competitive behaviour for mates or territories, typically accompanied by high T-levels, and investment in paternal care, typically accompanied by low T-levels. To test this hypothesis we monitored song activity, as a measure of territorial advertisement or mate attraction, and feeding efforts, as a measure of paternal care, in great tit Parus major males that either received T-filled or empty implants in the middle of the feeding phase, a period of high paternal commitment and low T-levels. In support of the trade-off hypothesis, T-implanted males sang significantly more than controls. However, we found no significant effect of the elevated T-levels on male and female feeding behaviour despite the large increase in T following implantation. Also, no short-term effects on male fitness were found. Taken together these results do not support the trade-off hypothesis. We discuss that the low overall responsiveness in our study might be related to a high fitness cost of neglecting offspring in favour of T-enhanced behaviour.

The cost of sexual coercion and heterospecific sexual harassment on the fecundity of a host-specific, seed-eating insect ( Neacoryphus bicrucis )

Two species of seed-eating true bugs, Neacoryphus bicrucis (Heteroptera: Lygaeidae) and Margus obscurator (Heteroptera: Coreidae) co-occur on ragwort, Senecio tomentosus, in southern Georgia, USA. Males of both species sometimes engage in chases and protracted grappling with females that flee initial mountings. Sometimes genital coupling occurs while the wriggling female is restrained in the male's grasp. Chases, grappling, and mounting attempts are misdirected toward heterospecific females, heterospecific males, or conspecific males. In a laboratory study, confinement of mated N. bicrucis females with either conspecific or heterospecific males reduced fecundity by approximately one-half relative to mated females confined only with other females. Perhaps as a consequence of this, N. bicrucis females frequently leave areas of high host plant density, where they prefer to oviposit, when males are abundant. The abundance of each species is positively correlated with host plant density but the two species rarely occur together on the same plants. This may be an effect of heterospecific courtship which induces the flight of N. bicrucis more than the flight of M. obscurator. The laboratory results suggest that copulations following chases and grappling represent sexual harassment, not a mechanism of active female choice for a vigorous mate. As sexual harassment imposes high fitness costs that favor abandonment of host plants, it may, when misdirected, incidentally limit habitat use by ecologically similar species.

SELECTION AND STRAIN SPECIFICITY OF COMPATIBILITY BETWEEN SNAIL INTERMEDIATE HOSTS AND THEIR PARASITIC SCHISTOSOMES.

Many theoretical models of host-parasite coevolution assume that variation in host resistance to parasite infection is, at least partially, genetically determined and specific to the strain of infecting parasite. However, very few experimental studies have been conducted to test this assumption in animal-parasite systems. Biomphalaria glabrata snails serve as the intermediate hosts of Schistosoma mansoni. Although some snails are resistant to infection, there is no evidence of fixation of resistance in field populations. Two possible explanations for this are high fitness costs associated with resistance and a dynamic coevolution between parasite and host, perhaps involving matching alleles or gene-for-gene interactions. Two strains of B. glabrata were artificially selected for either resistance or susceptibility to each of two strains of S. mansoni parasite for three generations. Third-generation snails were then were exposed to either the parasite strain to which they had been selected or to a different parasite strain. In both host strains, resistance and susceptibility (compatibility) were found to be heritable. Moreover, compatibility to one parasite strain was not associated with compatibility to another strain, implying no genetic trade-off. Our results are discussed in terms of potential mechanisms of resistance in this host-parasite system and their implications to general coevolutionary theory.

Management of fat reserves in tufted titmice ( Parus bicolor ): evidence against a trade-off with food hoards

Caching species can manage their energy supply by adjusting body fat, number of caches, or both. It has been hypothesized that because body fat has a higher fitness cost than caches, small food-hoarding birds respond to increased starvation risk by increasing the number of their caches rather than their fat load. This hypothesis predicts that when birds cannot cache they should compensate for the loss of external energy storage by (1) shifting the time of their daily body mass accumulation toward earlier in the day and (2) increasing the overall level of their fat reserves. During the winter of 1995–1996, we tested these predictions with a caching species, the tufted titmouse (Parus bicolor). Each of six experimental birds was fed a diet of uncachable sunflower seed powder for 6 days, preceded and followed by 6-day control periods during which they were fed cachable sunflower seeds. The daily pattern of body mass gain was unaffected by the opportunity to cache. Furthermore, when unable to cache, the birds did not increase either their mean daily body mass, body mass in the middle of the day, or evening body mass compared to the two control periods. These results argue against the hypothesis of a trade-off between fat reserves and food caches in tufted titmice, and suggest that fat reserves are managed independently of external food caches.

Nerve insensitivity resistance to pyrethroids in Heliothine Lepidoptera

A neurophysiological assay developed previously was used to assess the incidence of nerve insensitivity resistance to synthetic pyrethroids in field strains of Helicoverpa armigera. Almost 70% of individuals from a sample of a highly pyrethroid-resistant population from Jiangsu Province, China were nerve-insensitive. Subsequent selection resulted in a strain homogeneous for expression of this mechanism. Likewise, over 95% of a sample from a strain of the insects from Andhra Pradesh, India were nerve-insensitive and a homogeneous strain was developed. Development of a nerve-insensitive laboratory strain of Heliothis virescens was undertaken but homozygosity could not be obtained. It is suggested that high fitness costs may be associated with this mechanism. The incidence of nerve insensitivity in Heliothine pests is reviewed and the role of phenotypic expression assays in molecular studies highlighted.

POPULATION STRUCTURE AND DYNAMICS OF SELECTED GENES IN THE MOSQUITO CULEX PIPIENS.

To determine the outcome of the combined effects of gene flow, genetic drift, and selection on the evolution of insecticide-resistance genes in the mosquito Culex pipiens, samples were collected along three transects crossing treated and nontreated areas in northern Spain and southern France. Electrophoretic polymorphisms of five presumably neutral genes disclosed that differentiation among samples was low, and that both Wright F-statistics and Slatkin private-alleles methods provided a high estimate for Nm. In contrast, there was a strong differentiation in the distribution of resistance genes closely associated with insecticide treatments. These divergent situations are explained in relation to both the very recent origin of some resistance genes that are still localized geographically (A2-B2 and C1), and the high fitness cost of the older and ubiquitous ones in nontreated areas (A1, A4-B4, and AceR ).