On the adaptive accuracy of directional asymmetry in insect wing size

Subtle left-right biases are often observed in organisms with an overall bilateral symmetry. The evolutionary significance of these directional asymmetries remains uncertain, however, and scenarios of both developmental constraints and adaptation have been suggested. Reviewing the literature on asymmetry in insect wings, we analyze patterns of directional asymmetry in wing size to evaluate the possible adaptive significance of this character. We found that directional asymmetry in wing size is widespread among insects, with left- and right-biased asymmetries commonly observed. The direction of the asymmetry does not appear to be evolutionarily conserved above the species level. Overall, we argue that the very small magnitude of directional asymmetry, 0.7% of the wing size on average, associated with an extremely imprecise expression, precludes directional asymmetry from playing any major adaptive role.     

Specification of left-right asymmetry in the embryonic gut of Drosophila

Most animals exhibit stable left-right asymmetries in their body. Although significant progress has been made in elucidating the mechanisms that set up these asymmetries in vertebrates, nothing is known about them in Drosophila. This is usually attributed to the fact that no reversals of stable left-right asymmetries have been observed in Drosophila, although relevant surveys have been carried out. We have focused on the asymmetry of the proventriculus in the embryonic gut of Drosophila, an aspect of left-right asymmetry that is extremely stable in wild-type flies. We show that this asymmetry can be reversed by mutations in the dicephalic and wunen genes, which also cause reversals in the antero-posterior axis of the embryo relative to its mother. This is the first observation to suggest that left-right asymmetries in Drosophila can be reversed by genetic/developmental manipulations. It also suggests that maternal signals may initiate the specification of some left-right asymmetries in the embryo.     

Quantitative-genetic analysis of wing form and bilateral asymmetry in isochromosomal lines ofDrosophila subobscura using Procrustes methods

Fluctuating asymmetry (FA) is often used as a measure of underlying developmental instability (DI), motivated by the idea that morphological variance is maladaptive. Whether or not DI has evolutionary potential is a highly disputed topic, marred by methodological problems and fuzzy prejudices. We report here some results from an ongoing study of the effects of karyotype, homozygosity and temperature on wing form and bilateral asymmetry using isochromosomal lines ofDrosophila subobscura. Our approach uses the recently developed methodologies in geometric morphometrics to analyse shape configurations of landmarks within the standard statistical framework employed in studies of bilateral asymmetries, and we have extended these methods to partition the individual variation and the variation in asymmetries into genetic and environmental causal components. The analyses revealed temperaturedependent expression of genetic variation for wing size and wing shape, directional asymmetry (DA) of wing size, increased asymmetries at suboptimal temperature, and a transition from FA to DA in males as a result of increase in the rearing temperature. No genetic variation was generally detected for FA in our samples, but these are preliminary results because no crosses between lines were carried out and, therefore, the contribution of dominance was not taken into account. In addition, only a subset of the standing genetic variation was represented in the experiments.     

Thermal evolution of pre-adult life history traits, geometric size and shape, and developmental stability in Drosophila subobscura

Replicated lines of Drosophila subobscura originating from a large outbred stock collected at the estimated Chilean epicentre (Puerto Montt) of the original New World invasion were allowed to evolve under controlled conditions of larval crowding for 3.5 years at three temperature levels (13, 18 and 22 degrees C). Several pre-adult life history traits (development time, survival and competitive ability), adult life history related traits (wing size, wing shape and wing-aspect ratio), and wing size and shape asymmetries were measured at the three temperatures. Cold-adapted (13 degrees C) populations evolved longer development times and showed lower survival at the highest developmental temperature. No divergence for wing size was detected following adaptation to temperature extremes (13 and 22 degrees C), in agreement with earlier observations, but wing shape changes were obvious as a result of both thermal adaptation and development at different temperatures. However, the evolutionary trends observed for the wing-aspect ratio were inconsistent with an adaptive hypothesis. There was some indication that wing shape asymmetry has evolutionarily increased in warm-adapted populations, which suggests that there is additive genetic variation for fluctuating asymmetry and that it can evolve under rapid environmental changes caused by thermal stress. Overall, our results cast strong doubts on the hypothesis that body size itself is the target of selection, and suggest that pre-adult life history traits are more closely related to thermal adaptation.     

A new genus of long-legged flies displaying remarkable wing directional asymmetry

A previously unknown group of flies is described whose males exhibit directional asymmetry, in that the left wing is larger than, and of a different shape from, the right wing. To our knowledge, wing asymmetry of this degree has not previously been reported in an animal capable of flight. Such consistent asymmetry must result from a left-right axis during development, a level of differentiation whose existence has been questioned for insects. Wing asymmetry of this magnitude has implications for questions in areas of development, natural selection, flight, mate selection and communication in insects. The 'handicap principle' provides a possible explanation: females will choose a mate with the greatest handicap because his survival, in spite of his handicap, is a measure of his genetic superiority.     

Left–right asymmetries and shape analysis on Ceroglossus chilensis (Coleoptera: Carabidae)

Bilateral symmetry is widespread in animal kingdom, however most animal can deviate from expected symmetry and manifest some kind of asymmetries. Fluctuating asymmetry is considered as a tool for valuating developmental instability, whereas directional asymmetry is inherited and could be used for evaluating evolutionary development. We use the method of geometric morphometrics to analyze left/right asymmetries in the whole body, in two sites and totally six populations of Ceroglossus chilensis with the aim to infer and explain morphological disparities between populations and sexes in this species. In all individuals analyzed we found both fluctuating asymmetry and directional asymmetry for size and shape variation components, and a high sexual dimorphism. Moreover a high morphological variability between the two sites emerged as well. Differences in diet could influence the expression of morphological variation and simultaneously affect body sides, and therefore contribute to the symmetric component of variation. Moreover differences emerged between two sites could be a consequence of isolation and fragmentation, rather than a response to local environmental differences between sampling sites.     

Relationships between body size and sound‐producing structures in crickets: do large males have large harps?

Abstract. Male crickets produce conspicuous acoustic signals to attract mates and deter potential rivals. These signals are created when a male cricket closes his wings rapidly and a file and scraper mechanism causes several areas of the wing to vibrate. The harp is an area of the wing that is part of the resonating structure. Because the harp acts as part of a mechanical resonator, changes in harp area or mass could influence the frequency of sound produced. Because females exhibit stabilizing selection on the frequency used in male songs, we hypothesized that there would be a negative allometric relationship between body size and harp area. In addition, we examined the degree of asymmetry in the harp, wing, and tibia. We examined this in four different species of cricket: Acheta domesticus, Gryllus bimaculatus, Gryllus rubens , and Teleogryllus oceanicus. For each species, we measured pronotum width as an index of body size, tibia length, and the area of the forewing and harp. There were significant differences among species in their morphological characteristics. We observed consistent directional asymmetry in the harp area but not in the total wing area. When wings did exhibit directional asymmetry, it was in the opposite direction of the directional asymmetry observed in the harp. Within species, larger males typically had larger harps and the relationship between harp area and body size exhibited negative allometry. Wing area exhibited an isometric relationship with body size. Our data provide a potential mechanism linking decreases in song frequency with body size in male crickets, and suggest that sensory constraints might influence the morphology of signaling structures in a similar fashion as genitalia.     

Rhodnius prolixus and Rhodnius robustus–like (Hemiptera, Reduviidae) wing asymmetry under controlled conditions of population density and feeding frequency

Habitat change in Rhodnius spp may represent an environmental challenge for the development of the species, particularly when feeding frequency and population density vary in nature. To estimate the effect of these variables in stability on development, the degree of directional asymmetry (DA) and fluctuating asymmetry (FA) in the wing size and shape of R. prolixus and R. robustus–like were measured under laboratory controlled conditions. DA and FA in wing size and shape were significant in both species, but their variation patterns showed both inter-specific and sexual dimorphic differences in FA of wing size and shape induced by nutrition stress. These results suggest different abilities of the genotypes and sexes of two sylvatic and domestic genotypes of Rhodnius to buffer these stress conditions. However, both species showed non-significant differences in the levels of FA between treatments that simulated sylvan vs domestic conditions, indicating that the developmental noise did not explain the variation in wing size and shape found in previous studies. Thus, this result confirm that the variation in wing size and shape in response to treatments constitute a plastic response of these genotypes to population density and feeding frequency.     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

Left-right asymmetry: class I myosins show the direction

Myosins are actin-based molecular motors that are found in almost all eukaryotes. Phylogenetic analysis allows the discrimination of 37 different types of myosins, most with unknown functions. Recent work in Drosophila has revealed a crucial role for type ID unconventional myosin in left-right asymmetry. Mutations in Myosin ID completely reverse the left-right axis (situs inversus), a phenotype that is dependent on an intact actin cytoskeleton. How this myosin might orient the left-right axis has began to be elucidated by showing that it interacts directly with beta-catenin, suggesting that myosin ID interacts with the adherens junction to control the direction of organ looping. This is the first demonstration of a role of a myosin in body patterning.     

A three-tiered mechanism for regulation of planar cell polarity

Some epithelial cells are polarized along an axis orthogonal to their apical-basal axes. Recent studies in Drosophila lead to the view that three classes of signaling molecules govern the planar cell polarity (PCP) pathway. The first class, or module, functions across whole tissues, providing directional information to individual cells. The second module, apparently shared by all planar polarized tissues, and related to the canonical Wnt signaling pathway, interprets the directional signal to produce subcellular asymmetries. The third modules are tissue specific, acting to translate subcellular asymmetry into the appropriate morphological manifestations in the different cell types.     

Unveiling the establishment of left-right asymmetry in the chick embryo

Vertebrates display striking left-right asymmetries in the placement of internal organs, which are concealed by a seemingly bilaterally symmetric body plan. The establishment of asymmetries about the left-right axis occurs early during embryo development and requires the concerted and sequential action of several epigenetic, genetic and cellular mechanisms. Experiments in the chick embryo model have contributed crucially to our current understanding of such mechanisms and are reviewed here. Particular emphasis is given to the elucidation of a genetic network that conveys left-right information from Hensen's node to the organ primordia, characterized to a significant degree of detail in the chick embryo. We also point out a number of early and late events in the determination of left-right asymmetries that are currently poorly understood and for whose study the chick embryo model presents several advantages. We anticipate that the availability of the chick genome sequence will be combined with multidisciplinary approaches from experimental embryology, biophysics, live-cell imaging, and mathematical modeling to boost up our knowledge of left-right organ asymmetry in the near future.     

Adaptation and constraint in the evolution of Drosophila melanogaster wing shape

SUMMARY We have taken advantage of parallel instances of natural selection on body size in Drosophila melanogaster to investigate constraints and adaptation affecting wing shape. Using recently developed techniques for statistical shape analysis, we have examined variation in wing shape in similar body size clines on three continents. Gender-related shape differences were constant among all populations, suggesting that gender differences represent a developmental constraint on wing shape. In contrast, the underlying shape varied significantly between continents and shape change within each cline (i.e., between small and large body size populations) also varied between continents. Therefore, variation at these two levels presumably results from either drift or natural selection. Functional considerations suggest that shape variation between the continents is unlikely to be adaptive. However, cline-related shape change, which we show has a significant allometric component, may be adaptive. The overall range of wing shape variation, across a large range of wing size, is extremely small, and the possibility that wing shape is subject to stabilizing selection (or canalization) is discussed.     

Testis asymmetry and sperm length in Rhacophorus omeimontis

Theory predicts that the degree of testes asymmetry should be positively correlated with male body condition in species with directional testis asymmetry. We tested this prediction in Rhacophorus omeimontis, a species in which females mate with more than one male. Our results showed that the treefrogs did not exhibit the absence of directional asymmetry in testis size, but rather the occurrence of fluctuating asymmetry. Moreover, we also tested differences in body size, body mass, testis mass, testis asymmetry, and sperm size among initially paired, jointly paired, and unpaired males. We found that body size and mass, testis mass, testis asymmetry and sperm length did not differ among the three male types. Testis mass showed a positive relationship with soma mass, but the correlations between the extent of fluctuating testis asymmetry and sperm length, and between testis mass and sperm length were not significant. Our data suggest that testes size and sperm length do not play an important role in determining male mating success in the presence of sperm competition.     

Wing morphology and fluctuating asymmetry depend on the host plant in cactophilic Drosophila

As in most insect groups, host plant shifts in cactophilic Drosophila represent environmental challenges as flies must adjust their developmental programme to the presence of different chemical compounds and/or to a microflora that may differ in the diversity and abundance of yeasts and bacteria. In this context, wing morphology provides an excellent opportunity to investigate the factors that may induce changes during development. In this work, we investigated phenotypic plasticity and developmental instability of wing morphology in flies on the cactophilic Drosophila buzzatii and Drosophila koepferae raised on alternative breeding substrates. We detected significant differences in wing size between and within species, and between flies reared on different cactus hosts. However, differences in wing shape between flies emerged from different cactus hosts were not significant either in D. buzzatii or in D. koepferae. Our results also showed that morphological responses involved the entire organ, as variation in size and shape correlated between different portions of the wing. Finally, we studied the effect of the rearing cactus host on developmental instability as measured by the degree of fluctuating asymmetry (FA). Levels of FA in wing size were significantly greater in flies of both species reared in non-preferred when compared with those reared in preferred host cacti. Our results are discussed in the framework of an integrative view aimed at investigating the relevance of host plant shifts in the evolution of the guild of cactophilic Drosophila species that diversified in South America.     

Testis asymmetry in birds: the influences of sexual and natural selection

Gonad size and shape asymmetries are particularly common in birds. Although some obvious size and shape differences between the left and right testes in birds were first documented more than a century ago, little is known about what influences the variation across species in either the degree or the direction of these asymmetries. Here we show that a left bias in size is the most likely ancestral state in most orders and families, and that there is a weak but significant negative relation between the degree of size and shape asymmetries. In extant species, testis size and shape symmetries increase with the degree of sperm competition (relative testes mass), but those relations are significant only in those species with left bias in each of these traits. When space is particularly constrained on the left side of the body cavity due to a large gizzard (e.g. in granivores), the left testis is more elongated and the degree of size symmetry is larger. Despite significant patterns, relative testes mass and gizzard complexity together explain < 10% of the variation in testis asymmetry in species with left biases. Thus our analyses suggest that some other factor is largely responsible for the evolution of gonad asymmetry in birds: 1) that a left bias in testis size might be a correlated response to selection for a left bias in the development of a single (left) ovary in females of most bird species, and/or 2) that physiological efficiency due to the dramatic and rapid increase in testis size of most species during the breeding season might favour enlargement of one testis. Our conclusions highlight the need to rethink and improve our understanding of the physiological processes underlying the investment in gonads by male birds.     

How Useful is Fluctuating Asymmetry in Conservation Biology: Asymmetry in Rare and Abundant Coenonympha Butterflies

It has been suggested that minor, fluctuating differences in size of bilateral traits could validly indicate individual differences in developmental stability. One plausible reason for instability to occur could be lowered population size, which has been suggested to increase fluctuating asymmetry due to inbreeding, for example. We measured seven wing asymmetries of three Coenonympha butterfly species in central Sweden. One species is abundant (nobreak C. pamphilus), one rather common (C. arcania), and one rare (C. hero). We expected that if fluctuating asymmetry is a reliable indicator of population quality and thus a useful tool for conservation purposes, the most abundant species should show lowest asymmetry and the most endangered, the highest. Contrary to our expectations, the highest wing asymmetry was found in the relatively common species C. arcania and the most abundant and rare species did not show significant differences in levels of wing asymmetry. Our results obtained from three Coenonympha species hence suggest that the use of fluctuating asymmetry as an indicator of population conservation status may be misleading. Possible increase in asymmetry of small and/or isolated populations of butterflies may be masked by local differences in environmental conditions that could have high impact on bilateral development as well.     

Are wing size,wing shape and asymmetry related to field fitness of Trichogramma egg parasitoids?

The effects of wing shape, wing size, and fluctuating asymmetry in these measures on the field fitness of T. nr. brassicae and T. pretiosum were investigated. Trichogramma wasps mass-reared on eggs of the factitious host Sitotroga cerealella were released in tomato paddocks and those females ovipositing on Helicoverpa spp. eggs were recaptured. Comparisons of the recaptured group with a sample from the release population were used to assess fitness. Wing data were obtained by positioning landmarks on mounted forewings. Size was then measured as the centroid size computed from landmark distances, while Procrustes analysis followed by principal component analysis was used to assess wing shape. Similar findings were obtained for both Trichogramma species: fitness of wasps was strongly related to wing size and some shape dimensions, but not to the asymmetries of these measures. Wasps which performed well in the field had larger wings and a different wing shape compared to wasps from the mass reared population. Both size and the shape dimensions were linearly associated with fitness although there was also some evidence for non-linear selection on shape. The results suggest that wing shape and wing size are reliable predictors of field fitness for these Trichogramma wasps.