Bias in the heritability of preference and its potential impact on the evolution of mate choice.

The evolution of mate choice is a function of the heritability of preference. Estimation in the laboratory is typically made by presenting a female with a limited number of males. We show that such an approach produces a downwardly biased estimate, which we term the heritability of choice. When preference is treated as a threshold trait then less biased estimates are obtained particularly for preferences based on the relative value of the preferred trait. Because females in the wild typically survey on average less than five males we argue that the heritability of choice may be more meaningful than the heritability of preference. The restricted number of males surveyed can lead to a reduction in the phenotypic variance of the preferred trait in the group of males selected by the females if the phenotypic variance in preference is equal to or less than the phenotypic variance in the referred trait. If the phenotypic variance in preference exceeds that of the preferred trait then the opposite occurs. A second effect of the restricted number of males sampled is that females are likely to mate initially with males that are not the most preferred. The failure to find the most preferred male may account for the common observation of multiple matings and extra-pair copulations. We suggest that current explanations for polyandry need to take this failure into account.

The costs of being dark: the genetic basis of melanism and its association with fitness-related traits in the sand cricket.

Melanism is an important component of insect cuticle and serves numerous functions that enhance fitness. Despite its importance, there is little information on its genetic basis or its phenotypic and genetic correlation with fitness-related traits. Here, we examine the heritability of melanism in the wing dimorphic sand cricket and determine its phenotypic and genetic correlation with wing morphology, gonad mass and size of the dorso-longitudinal muscles (the principle flight muscles). Previously demonstrated trade-offs among these traits are significant factors in the evolution of life history variation. Using path analysis, we show that melanization is causally related to gonad mass, but not flight muscle mass. Averaged over the sexes, the heritability of melanism was 0.61, the genetic correlation with gonad mass was -0.36 and with wing morph was 0.51. The path model correctly predicted the ranking of melanization score in lines selected for increased ovary mass, increased flight muscle mass, an index that increased both traits and an unselected control. Our results support the general hypothesis that melanization is costly for insects and negatively impacts investment in early reproduction.

Path analysis of the genetic integration of traits in the sand cricket: a novel use of BLUPs.

This study combines path analysis with quantitative genetics to analyse a key life history trade-off in the cricket, Gryllus firmus. We develop a path model connecting five traits associated with the trade-off between flight capability and reproduction and test this model using phenotypic data and estimates of breeding values (best linear unbiased predictors) from a half-sibling experiment. Strong support by both types of data validates our causal model and indicates concordance between the phenotypic and genetic expression of the trade-off. Comparisons of the trade-off between sexes and wing morphs reveal that these discrete phenotypes are not genetically independent and that the evolutionary trajectories of the two wing morphs are more tightly constrained to covary than those of the two sexes. Our results illustrate the benefits of combining a quantitative genetic analysis, which examines statistical correlations between traits, with a path model that focuses upon the causal components of variation.

Trade-off acquisition and allocation in Gryllus firmus: a test of the Y model.

Many models of life history evolution assume trade-offs between major life history traits; however, these trade-offs are often not found. The Y model predicts that variation in acquisition can mask underlying allocation trade-offs and is a major hypothesis explaining why negative relationships are not always found between traits that are predicted to trade-off with one another. Despite this model's influence on the field of life history evolution, it has rarely been properly tested. We use a model system, the wing dimorphic cricket, Gryllus firmus as a case study to test the assumptions and predictions of the Y model. By experimentally altering the acquisition regime and by estimating energy acquisition and energy allocation directly in this species, we are able to explicitly test this important model. Overall, we find strong support for the predictions of the Y model.

Why do Californian striders fly?

Discerning the adaptive significance of migratory strategies poses significant challenges, not the least of which is measuring migratory capability in natural populations. We take advantage of a visible migratory dimorphism to study variation in migratory capability in the stream-dwelling water strider, Aquarius remigis. Theory predicts loss of migratory capability in this species because streams have been viewed as stable and persistent habitats. As expected, A. remigis lack wings throughout most of North America. However, Californian populations are noted for unexpectedly high frequencies of winged, migratory morphs. To deduce the adaptive significance of this anomalous regional variation, we compare proportion winged among 37 Californian populations. We discover a strong, positive correlation with altitude, but no correlations with latitude, rainfall or stream size. A common garden experiment reveals that both proportion winged and its reaction norm to temperature differ genetically among populations, and a half-sibling experiment demonstrates that wing morph has high heritability, moderate genetic correlations across environments and a significant genotype by environment interaction. These results support the hypothesis that proportion winged and its reaction norm to temperature have diverged genetically in California. We conclude that high migratory capability is an evolutionary adaptation to the unusual harshness and instability of Californian stream habitats, and particularly to the high elevational gradients and extreme seasonal variation characteristic of montane streams.

Male sand crickets trade-off flight capability for reproductive potential.

In this paper, we test the hypothesis that male sand crickets, Gryllus firmus, experience a trade-off between flight capability and reproductive potential expressed as reduced testis weight in flight-capable morphs. We used a half-sib design with 130 sires, three dams per sire and an average of 5.66 males per dam family, for a total of 2206 F1 offspring. Traits measured were head width, somatic dry weight, testis weight, wing morph (micropterous/macropterous), weight of the dorso-longitudinal flight muscles (DLM) and the functional status of these muscles. Heritabilities of all traits were significant and ranged from 0.14 to 0.43. All traits were positively correlated with body size, but removal of this covariance revealed a highly significant trade-off, both phenotypically and genetically, between testes size and flight capability as measured by wing morph, DLM size or DLM status. The possible implications of this for morph-specific reproductive tactics are discussed.

The evolution of trade-offs: where are we?

Trade-offs are a core component of many evolutionary models, particularly those dealing with the evolution of life histories. In the present paper, we identify four topics of key importance for studies of the evolutionary biology of trade-offs. First, we consider the underlying concept of 'constraint'. We conclude that this term is typically used too vaguely and suggest that 'constraint' in the sense of a bias should be clearly distinguished from 'constraint' in the sense of proscribed combinations of traits or evolutionary trajectories. Secondly, we address the utility of the acquisition-allocation model (the 'Y-model'). We find that, whereas this model and its derivatives have provided new insights, a misunderstanding of the pivotal equation has led to incorrect predictions and faulty tests. Thirdly, we ask how trade-offs are expected to evolve under directional selection. A quantitative genetic model predicts that, under weak or short-term selection, the intercept will change but the slope will remain constant. Two empirical tests support this prediction but these are based on comparisons of geographic populations: more direct tests will come from artificial selection experiments. Finally, we discuss what maintains variation in trade-offs noting that at present little attention has been given to this question. We distinguish between phenotypic and genetic variation and suggest that the latter is most in need of explanation. We suggest that four factors deserving investigation are mutation-selection balance, antagonistic pleiotropy, correlational selection and spatio-temporal variation, but as in the other areas of research on trade-offs, empirical generalizations are impeded by lack of data. Although this lack is discouraging, we suggest that it provides a rich ground for further study and the integration of many disciplines, including the emerging field of genomics.

The quantitative genetics of sexual dimorphism: assessing the importance of sex-linkage.

Sexual dimorphism (SD) is a defining feature of gonochorous animals and dioecious plants, but the evolution of SD from an initially monomorphic genome presents a conundrum. Theory predicts that the evolution of SD will be facilitated if genes with sex-specific fitness effects occur on sex chromosomes. We review this theory and show that it generates three testable predictions. For organisms with an XX/XY chromosomal system of sex determination: (1) SD should be associated with X-linked effects; (2) X-linked effects should show strong directional dominance for sexually dimorphic traits favored in males but expressed in both sexes; and (3) SD should be associated with a reduction in the between-sex additive genetic covariance and correlation. A literature review reveals that empirical evaluations of the association between sex-linkage and SD have lagged behind theory. Tests for the presence of sex-linked effects have been plagued by the need to make simplifying assumptions, such as the absence of dominance or maternal effects, that greatly weaken their discriminatory power. Further, most have used comparisons between species or populations, whereas the correct level of analysis is within populations. To overcome these problems, we derive a novel pedigree design that permits separate estimation of X-linked, dominance and maternal effects. We suggest that the data from such a design would be most appropriately analyzed using the animal model. This novel protocol will allow quantitative evaluation of the above predictions, and hence should spur progress in understanding the role of sex-linkage in the evolution of SD.

One tool, many uses: precopulatory sexual selection on genital morphology in Aquarius remigis.

While congruent evidence indicates that sexual selection is the most likely selective force explaining the rapid divergence of male genital morphology in insects, the mechanisms involved in this process remain unclear. In particular, little attention has been paid to precopulatory sexual selection. We examine sexual selection for mating success on male genital components in six populations of Aquarius remigis, a water strider characterized by unique genital morphology. Multivariate selection analysis confirms previous findings that precopulatory sexual selection favours longer external genitalia, and provides new evidence that this selection acts independently on external genital components. In contrast, the size of the major internal genital sclerite is not correlated with mating success. Thus, precopulatory sexual selection acts strongly on the size of the external genitalia, but not on the intromittent organ itself. These results highlight the multiple functions of genital organs and the importance of both precopulatory and post-copulatory sexual selection in shaping the remarkable diversity of male genitalia in insects.

Competing dwarf males: sexual selection in an orb-weaving spider.

Hypotheses for the adaptive significance of extreme female-biased sexual size dimorphism (SSD) generally assume that in dimorphic species males rarely interfere with each other. Here we provide the first multivariate examination of sexual selection because of male-male competition over access to females in a species with 'dwarf' males, the orb-weaving spider Argiope aurantia. Male A. aurantia typically try to mate opportunistically during the female's final moult when she is defenceless. We show that, contrary to previous hypotheses, the local operational sex ratio (males per female on the web) is male-biased most of the season. Both interference and scramble competition occur during opportunistic mating, the former leading to significant selection for large male body size. Male condition and leg length had no effect on mating success independent of size. We discuss these findings in the context of the evolution of extreme female-biased SSD in this clade.

The evolution of trade-offs: geographic variation in call duration and flight ability in the sand cricket, Gryllus firmus.

Quantitative genetic theory assumes that trade-offs are best represented by bivariate normal distributions. This theory predicts that selection will shift the trade-off function itself and not just move the mean trait values along a fixed trade-off line, as is generally assumed in optimality models. As a consequence, quantitative genetic theory predicts that the trade-off function will vary among populations in which at least one of the component traits itself varies. This prediction is tested using the trade-off between call duration and flight capability, as indexed by the mass of the dorsolateral flight muscles, in the macropterous morph of the sand cricket. We use four different populations of crickets that vary in the proportion of macropterous males (Lab = 33%, Florida = 29%, Bermuda = 72%, South Carolina = 80%). We find, as predicted, that there is significant variation in the intercept of the trade-off function but not the slope, supporting the hypothesis that trade-off functions are better represented as bivariate normal distributions rather than single lines. We also test the prediction from a quantitative genetical model of the evolution of wing dimorphism that the mean call duration of macropterous males will increase with the percentage of macropterous males in the population. This prediction is also supported. Finally, we estimate the probability of a macropterous male attracting a female, P, as a function of the relative time spent calling (P = time spent calling by macropterous male/(total time spent calling by both micropterous and macropterous male). We find that in the Lab and Florida populations the probability of a female selecting the macropterous male is equal to P, indicating that preference is due simply to relative call duration. But in the Bermuda and South Carolina populations the probability of a female selecting a macropterous male is less than P, indicating a preference for the micropterous male even after differences in call duration are accounted for.

Characterization of two HKT1 homologues from Eucalyptus camaldulensis that display intrinsic osmosensing capability.

Plants have multiple potassium (K(+)) uptake and efflux mechanisms that are expressed throughout plant tissues to fulfill different physiological functions. Several different classes of K(+) channels and carriers have been identified at the molecular level in plants. K(+) transporters of the HKT1 superfamily have been cloned from wheat (Triticum aestivum), Arabidopsis, and Eucalyptus camaldulensis. The functional characteristics as well as the primary structure of these transporters are diverse with orthologues found in bacterial and fungal genomes. In this report, we provide a detailed characterization of the functional characteristics, as expressed in Xenopus laevis oocytes, of two cDNAs isolated from E. camaldulensis that encode proteins belonging to the HKT1 superfamily of K(+)/Na(+) transporters. The transport of K(+) in EcHKT-expressing oocytes is enhanced by Na(+), but K(+) was also transported in the absence of Na(+). Na(+) is transported in the absence of K(+) as has been demonstrated for HKT1 and AtHKT1. Overall, the E. camaldulensis transporters show some similarities and differences in ionic selectivity to HKT1 and AtHKT1. One striking difference between HKT1 and EcHKT is the sensitivity to changes in the external osmolarity of the solution. Hypotonic solutions increased EcHKT induced currents in oocytes by 100% as compared with no increased current in HKT1 expressing or uninjected oocytes. These osmotically sensitive currents were not enhanced by voltage and may mediate water flux. The physiological function of these osmotically induced increases in currents may be related to the ecological niches that E. camaldulensis inhabits, which are periodically flooded. Therefore, the osmosensing function of EcHKT may provide this species with a competitive advantage in maintaining K(+) homeostasis under certain conditions.

Estimating genetic correlations from measurements of field-caught waterstriders.

Lynch (1999) proposed a method for estimation of genetic correlations from phenotypic measurements of individuals for which no pedigree information is available. This method assumes that shared environmental effects do not contribute to the similarity of relatives, and it is expected to perform best when sample sizes are large, many individuals in the sample are paired with close relatives, and heritability of the traits is high. We tested the practicality of this method for field biologists by using it to estimate genetic correlations from measurements of field-caught waterstriders (Aquarius remigis). Results for sample sizes of less than 100 pairs were often unstable or undefined, and even with more than 500 pairs only half of those correlations that had been found to be significant in standard laboratory experiments were statistically significant in this study. Statistically removing the influence of environmental effects (shared between relatives) weakened the estimates, possibly by removing some of the genetic similarity between relatives. However, the method did generate statistically significant estimates for some genetic correlations. Lynch (1999) anticipated the problems found, and proposed another method that uses estimates of relatedness between members of pairs (from molecular marker data) to improve the estimates of genetic correlations, but that approach has yet to be tested in the field.

Characterisation of two distinct HKT1-like potassium transporters from Eucalyptus camaldulensis.

Potassium is an essential macronutrient in higher plants. It plays an important physiological role in stoma movements, osmoregulation, enzyme activation and cell expansion. The demand for potassium can be substantial, especially when the plant concerned is a Eucalyptus tree in excess of 50 m tall. We have isolated two cDNAs, EcHKT1 and EcHKT2, from Eucalyptus camaldulensis (river red gum) which are expressed in leaves, stems and roots. These encode potassium transporter polypeptides with homology to the wheat K+-Na+ symporter, HKT1. EcHKT1 and EcHKT2 both complemented the K+-limited growth of an Escherichia coli K+-uptake-deficient triple mutant. EcHKT1 and EcHKT2 also mediated Na+ and K+ uptake when expressed in Xenopus oocytes. A comparison of the EcHKT1 and EcHKT2 sequences and their transport properties indicated that these cDNAs represent two K+ transporters with distinct functional characteristics. The functional and structural conservation between these two E. camaldulensis genes and the wheat HKT1 suggests that they play an important, albeit elusive, physiological role.

Lifetime selection on adult body size and components of body size in a waterstrider: opposing selection and maintenance of sexual size dimorphism.

Sexual size dimorphism (SSD), the difference in body size between males and females, is common in almost all taxa of animals and is generally assumed to be adaptive. Although sexual selection and fecundity selection alone have often been invoked to explain the evolution of SSD, more recent views indicate that the sexes must experience different lifetime selection pressures for SSD to evolve and be maintained. We estimated selection acting on male and female adult body size (total length) and components of body size in the waterstrider Aquarius remigis during three phases of life history. Opposing selection pressures for overall body size occurred in separate episodes of fitness for females in both years and for males in one year. Specific components of body size were often the targets of the selection on overall body size. When net adult fitness was estimated by combining each individual's fitnesses from all episodes, we found stabilizing selection in both sexes. In addition, the net optimum overall body size of males was smaller than that of females. However, even when components of body size had experienced opposing selection pressures in individual episodes, no components appeared to be under lifetime stabilizing selection. This is the first evidence that contemporary selection in a natural population acts to maintain female size larger than male size, the most common pattern of SSD in nature.

Differential regulation of plastidial and cytosolic isoforms of peptide methionine sulfoxide reductase in Arabidopsis.

We report the characterization of two members of a gene family from Arabidopsis that encode, respectively, cytosolic (cPMSR) and plastid-targeted (pPMSR) isoforms of the oxidative-stress-repair enzyme peptide methionine sulfoxide reductase. Overexpression of these proteins in Escherichia coli confirmed that each had PMSR enzyme activity with a synthetic substrate, N-acetyl-[(3)H]-methionine sulfoxide, or a biological substrate, alpha-1 proteinase inhibitor. The pPMSR was imported into intact chloroplasts in vitro with concomitant cleavage of its approximately 5-kD N-terminal signal peptide. The two PMSR isoforms exhibited divergent pH optima, tissue localization, and responses to developmental and environmental effects. Analysis of the Arabidopsis database indicated that there are probably at least two p-pmsr-like genes and three c-pmsr-like genes in the Arabidopsis genome. Expression of the p-pmsr genes and their protein products was restricted to photosynthetic tissues and was strongly induced following illumination of etiolated seedlings. In contrast, the c-pmsr genes were expressed at moderate levels in all tissues and were only weakly affected by light. Exposure to a variety of biotic and abiotic stresses showed relatively little effect on pmsr gene expression, with the exception of leaves subjected to a long-term exposure to the cauliflower mosaic virus. These leaves showed a strong induction of the c-pmsr gene after 2 to 3 weeks of chronic pathogen infection. These data suggest novel roles for PMSR in photosynthetic tissues and in pathogen defense responses in plants.

Change in sexual size dimorphism as a correlated response to selection on fecundity.

Fecundity selection is often suggested as the main causal factor underlying the prevalence of female-biased sexual size dimorphism (SSD), but this assumption has not been empirically tested. We selected female Drosophila melanogaster for increased or decreased fecundity (eggs laid over a single 18-h period, between days 5 and 7 posteclosion) for 20 generations, to see what effect this would have on SSD in three morphological traits (thorax width, abdomen width and thorax length). A direct response to fecundity selection was found in the downward direction (16.6%), whereas the response to upward selection (5.7%) was not statistically significant. Significant sex by selection interaction terms in the ANOVAs for thorax width and abdomen width indicate that the two sexes responded differently. Females usually showed a greater correlated response than males. In lines selected for increased fecundity, the correlated response in females for thorax and abdomen width was greater than the direct response in standard deviation units. SSD generally increased with selection for increased fecundity, but showed no consistent trend with selection for decreased fecundity. These results support the general hypothesis that SSD can evolve rapidly in response to fecundity selection. Selection on fecundity also produced correlated responses in life history traits. Downward selection resulted in flies that had lower viability and longevity, and both directions of selection were associated with an increase in development time.

Patterns of postmating reproductive isolation in a newly discovered species pair, Aquarius remigis and A. remigoides (Hemiptera;Gerridae).

Aquarius remigoides Gallant and Fairbairn has recently been described as specifically distinct from A. remigis (Say) based upon genetic and morphological data. Both species are common, semiaquatic bugs (Hemiptera; Gerridae) found on the surface of streams and small rivers. Allozyme studies have shown them to be more distantly related than most other congeneric species in the Gerridae, with significant barriers to gene flow where their ranges abut. We assess postmating reproductive isolation between A. remigoides and A. remigis, using a bracket cross design with five sampling sites along a north-south cline traversing the hybrid zone. We also report the results of long-distance conspecific crosses of A. remigis, using populations from California and Quebec. Neither these nor the intraspecific bracket crosses reveal any evidence of isolation by distance within species. However, heterospecific crosses show significantly reduced fertility, hatching success, survival of both sexes to eclosion (final moult) and percentage of males. Egg production is not influenced by cross type, and we found no evidence of hybrid sterility in either sex. Analyses of genotypic frequencies at three isozyme loci in eight hybrid and 22 pure populations reveal significant deficiencies of heterozygotes in hybrid populations. The proportion of males is also significantly lower in hybrid populations than in pure populations. The laboratory and field results indicate that postmating isolation between these two species occurs in the form of severe reductions in both the fertility of heterospecific crosses and the viability of hybrids, particularly hybrid males. Genetic mechanisms for Haldane's rule and asymmetries in the reciprocal heterospecific crosses are discussed.

Identification of a peptide methionine sulphoxide reductase gene in an oleosin promoter from Brassica napus.

A bidirectional promoter can be defined operationally as a short segment of DNA that regulates divergent transcription. In an attempt to investigate whether the intergenic region between the oleosin and a second open reading frame (ORFII) in Brassica napus (L.) is a divergent promoter, and also to characterize the ORFII, cDNA clones homologous to ORFII were isolated from a leaf cDNA library. A representative cDNA (clone D) of one of the two classes identified was identical, in DNA sequence, to the genomic ORFII. The second representative cDNA (clone O) was 97% identical at the nucleotide level to the genomic ORFII. The predicted amino acid sequence of the cDNA clones each exhibit homology with the peptide methionine sulphoxide reductase (PMSR) of Escherichia coli. The gene structure of ORFII was elucidated and the relative positions of the oleosin, ORFII, and the intergenic promoter region were determined. This confirms that the B. napus oleosin-ORFII intergenic region has divergent promoter activity. Consequently this is the first such plant nuclear divergent promoter identified. RFLP-mapping results showed that all four ORFII genes are linked to four of the six copies of the oleosin genes. This suggested that the bidirectional promoter locus is conserved within the B. napus genome. The ORFII gene product is targeted to the chloroplast, which is consistent with previous data indicating the presence of PMSR activity in the chloroplast. The over-expressed recombinant fusion protein (minus the transitpeptide) showed the capability to reduce peptide methionine sulphoxide residues in vitro, indicating PMSR activity. This study demonstrates that ORFII is transcribed and encodes a plant PMSR, and is the first example of the isolation of a eukaryotic PMSR gene.

THE EVOLUTION OF ALTERNATE MORPHOLOGIES: FITNESS AND WING MORPHOLOGY IN MALE SAND CRICKETS.

Many organisms show distinct morphological types. We argue that the evolution of these alternate morphologies depends upon both fitness differences between morphs within each sex and the genetic correlation between sexes. In this paper, we examine the evolution of alternate morphologies using wing dimorphism in insects as a model system. Many insect species are wing dimorphic, one morph having wings and being capable of flight, the other lacking functional wings. While there is a well established trade-off in females between macroptery and reproduction, there are few data on the possible costs in males. We examine trade-offs between macroptery and life-history traits in male sand crickets, Gryllus firmus, and estimate the genetic correlation of wing dimorphism between the sexes. Macropterous males develop faster than micropterous males and are either larger or the same size depending upon rearing conditions. There is no difference in absolute or relative testis size at eclosion or 7 d thereafter. Finally, there is no difference between macropterous and micropterous males in relative success at siring offspring. Thus, with respect to the above traits, there are no costs associated with being winged in male G. firmus. It is possible that there may be a trade-off between calling rate and macroptery. A comparison of the relative frequency of macroptery between males and female across different orders of insects supports this hypothesis. The genetic correlation of wing dimorphism between the sexes is high (r8 = 0.86), and hence the frequency of macroptery in males may be strongly influenced by selection acting on females.