Fluctuating asymmetry in certain morphological traits in laboratory populations of Drosophila ananassae.

Fluctuating asymmetry (FA, subtle random deviations from perfect bilateral symmetry) is often used as a measure of developmental instability (DI), which results from perturbations in developmental pathways caused by genetic or environmental stressors. During the present study, we estimated FA in 5 morphological traits, viz. wing length (WL), wing to thorax ratio (W:T), sternopleural bristle number (SBN), sex-comb tooth number (SCTN), and ovariole number (ON) in 18 laboratory populations of Drosophila ananassae. FA levels of measured traits differed significantly among populations except for SBN (in males and females) and W:T ratio (in females). Positional fluctuating asymmetry (PFA), a sensitive measure of DI, also varied significantly among the populations for SBN in females and SCTN in males. Interestingly, both males and females were similar for nonsexual traits. However, when FA across all traits (sexual and nonsexual) was combined into a single composite index (CFA), significant differences were found for both populations and sexes. Males showed higher CFA values than females, suggesting that males are more prone to developmental perturbations. The magnitude of FA differed significantly among traits, being lowest for nonsexual traits (SBN, WL, W:T ratio) and highest for sexual traits (SCTN and ON). The trait size of sexual traits (SCTN and ON) was positively correlated with their asymmetry. The possible reasons for variation in FA both among traits and among populations, and the usefulness of FA as an indicator of developmental stress and phenotypic quality in D. ananassae are discussed.     

Effect of mutations on developmental stability and canalization in morphological traits in Drosophila ananassae

The present study was designed to determine the effects of visible mutations of large effect on developmental stability and canalization in different morphological traits, namely, sternopleural bristle number, wing length, wing to thorax ratio, ovariole number, and sex comb tooth number (SCTN) in Drosophila ananassae. We have compared the mean trait size, fluctuating asymmetry (FA) (as an index of developmental stability), and morphological variation (as an index of canalization) of different mutant strains (yellow body color, y; claret eye color, ca; plexus wing, px; spread wing, spr; ebony body and sepia eye color, e se; yellow body and claret eye color, y ca; and cardinal eye color, curled wing, and ebony body color, cd cu e) with wild-type strain. The mean trait size of all morphological traits differs significantly among the wild-type and mutant strains. The wild-type and mutant strains vary significantly for the morphological variation and also for the levels of the FA in different morphological traits. However, we have found no increase in either the variance or in the degree of FA with the increase of the mutations (except in SCTN in y mutant). The plausible reasons for the variation in wild-type and mutant strains with particular reference to developmental stability and canalization have been discussed.     

Effect of developmental temperature stress on fluctuating asymmetry in certain morphological traits in Drosophila ananassae

In the present study, the effect of thermal stress on the variability and fluctuating asymmetry (FA) in different morphological traits, viz., thorax length (TL), sternopleural bristle number (SBN), wing length (WL), wing-to-thorax (W/T) ratio, sex comb tooth number (SCTN) and ovariole number (ON), was investigated in 10 isofemale lines of Drosophila ananassae. The phenotypic and genetic variability is higher in the flies reared at low (20 °C) and at high (30 °C) temperatures as compared to that of standard (25 °C) temperature. Further, the levels of FA of measured traits differed significantly among the three temperature regimes except SBN and SCTN in males and SBN and W/T ratio in females. Moreover, the magnitude of positional fluctuating asymmetry is similar in males reared at three different developmental temperatures for SBN and SCTN but it varies significantly for SBN in females. However, when FA across all the traits was combined into a composite index (CFA), significant differences were found for both temperature regimes and sexes. Males showed higher CFA at 30 °C whereas in females it was higher at 20 °C. The results suggest that temperature increases the levels of variability and FA but the effect seems to be trait and sex specific in D. ananassae.     

Outbreeding causes developmental instability in <Emphasis Type="Italic">Drosophila subobscura</Emphasis>

A possible effect of interpopulation hybridization is either outbreeding depression, as a consequence of breakdown of coadapted gene complexes which can increase developmental instability (DI) of the traits, or increased heterozygosity, which can reduce DI. One of the principal methods commonly used to estimate DI is the variability of fluctuating asymmetry (FA). We analysed the effect of interpopulation hybridization in Drosophila subobscura through the variability in the wing size and the FA of wing length and width for both sexes in parental, F1 and F2 generations. The results of the wing size per se in intra- and interpopulation hybrids of D. subobscura do not explicitly reveal the significance of either of the two hypotheses. However, the results of the FA of the wing traits give a different insight. The FA of wing length and width generally increases in interpopulation crosses in F1 with respect to the FA in the parental generation, which suggests the possibility that outbreeding depression occurred in the first generation after the hybridization event. We generally observed that the FA values for the wing length and width of interpopulation hybrids were higher in F1 and F2 generations, compared to intrapopulation hybrids in same generations. These results suggest that the association between coadaptive genes with the same evolutionary history are the most probable mechanism that maintains the developmental homeostasis in Drosophila subobscura populations.     

Hybridization, developmental stability, and functionality of morphological traits in the ground beetle Carabus solieri (Coleoptera, Carabidae)

The assessment of developmental stability in hybrids can provide valuable information in the study of species formation because it allows an evaluation of the degree of incompatibility of genetic systems that control developmental processes. The present study assessed the impact of two hybridization events, assumed to have occurred at different times, on developmental instability in the ground beetle Carabus solieri . Developmental instability was estimated in 678 individuals from 27 populations from the fluctuating asymmetry (FA) levels of four morphological traits: the tibia length of middle and hind legs, which are functional structures, and the length and the proximal width of the hind wings, which are vestigial and thus nonfunctional structures. Significant variations of FA levels between populations were shown only for the wing width. For this trait, FA levels in hybrids were higher than in their parental entities for both hybridization events, indicating a significant divergence of the gene systems controlling development between the parental entities in the two hybridization cases. As expected, wing traits exhibited FA levels at least three times higher than leg trait. Finally, the potential interest of vestigial traits in the particular context of hybridization is discussed.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 151–158.     

Multifaceted,Cross-Generational Costs of Hybridization in Sibling Drosophila species

Maladaptive hybridization, as determined by the pattern and intensity of selection against hybrid individuals, is an important factor contributing to the evolution of prezygotic reproductive isolation. To identify the consequences of hybridization between Drosophila pseudoobscura and D. persimilis, we estimated multiple fitness components for F1 hybrids and backcross progeny and used these to compare the relative fitness of parental species and their hybrids across two generations. We document many sources of intrinsic (developmental) and extrinsic (ecological) selection that dramatically increase the fitness costs of hybridization beyond the well-documented F1 male sterility in this model system. Our results indicate that the cost of hybridization accrues over multiple generations and reinforcement in this system is driven by selection against hybridization above and beyond the cost of hybrid male sterility; we estimate a fitness loss of >95% relative to the parental species across two generations of hybridization. Our findings demonstrate the importance of estimating hybridization costs using multiple fitness measures from multiple generations in an ecologically relevant context; so doing can reveal intense postzygotic selection against hybridization and thus, an enhanced role for reinforcement in the evolution of populations and diversification of species.     

Host use and developmental instability in the cactophilic sibling species Drosophila gouveai and D. antonietae

The Drosophila repleta group encompasses an ensemble of species that inhabit desertic areas that are inhospitable to other drosophilids. These species have a tractable ecology, as they breed and feed on necrotic tissues of a wide diversity of species of Cactaceae, with a certain degree of host specificity, which makes them suitable models to investigate the role of host plant shifts in diversification. Most species have their own primary host plant, which may be shared with a closely related species. However, the consequences of host plant shifts from primary to secondary hosts have not been thoroughly studied so far. We investigated the effects of the cactus host on developmental instability and performance of D. gouveai Tidon‐Sklorz & Sene and D. antonietae Tidon‐Sklorz & Sene (Diptera: Drosophilidae), a pair of closely related sibling species, and of their F1 interspecific hybrids reared in primary and secondary host plants. Fluctuating asymmetry (FA) for wing size was significantly greater in flies of both species reared in their respective secondary cactus host than in those grown in the primary host. Interspecific hybrids also exhibited host‐dependent levels of FA. However, hybrids did not show greater FA than the parental species, suggesting that hybridization per se did not affect developmental stability. Even though cactus host shifts affected different measures of fitness (larval viability and adult size) both in D. antonietae and D. gouveai, we did not detect a consistent relationship between FA and fitness. Our results suggest that FA cannot be used as a sensitive indicator of genetic and phenotypic quality and we discuss its application as a fitness predictor.     

Developmental stability in hybrids between the sibling species pair,Drosophila melanogaster and Drosophila simulans

Drosophila melanogaster and its sibling species D. simulans were hybridized in the laboratory to test the hypothesis that developmental homeostasis in hybrids between two species having no prior gene flow would be significantly reduced. Developmental stability was assessed by measuring fluctuating asymmetry for three bilateral traits: sternopleural chaetae, wing length, and fronto-orbital plus frontal chaetae. Male F₁ hybrids showed no decrease in developmental stability compared to males of parental species. Female hybrids showed significant fluctuating asymmetry compared to other flies. The results are discussed with respect to ideas about coadaptation and gene flow based upon previous studies of hybrid developmental stability.     

Symmetry breaking in interspecific Drosophila hybrids is not due to developmental noise

Hybrids from crosses of different species have been reported to display decreased developmental stability when compared to their pure species, which is conventionally attributed to a breakdown of coadapted gene complexes. Drosophila subobscura and its close relative D. madeirensis were hybridized in the laboratory to test the hypothesis that genuine fluctuating asymmetry, measured as the within-individual variance between right and left wings that results from random perturbations in development, would significantly increase after interspecific hybridization. When sires of D. subobscura were mated to heterospecific females following a hybrid half-sib breeding design, F1 hybrid females showed a large bilateral asymmetry with a substantial proportion of individuals having an asymmetric index larger than 5% of total wing size. Such an anomaly, however, cannot be plainly explained by an increase of developmental instability in hybrids but is the result of some aberrant developmental processes. Our findings suggest that interspecific hybrids are as able as their parents to buffer developmental noise, notwithstanding the fact that their proper bilateral development can be harshly compromised. Together with the low correspondence between the co-variation structures of the interindividual genetic components and the within-individual ones from a Procrustes analysis, our data also suggest that the underlying processes that control (genetic) canalization and developmental stability do not share a common mechanism. We argue that the conventional account of decreased developmental stability in interspecific hybrids needs to be reappraised.     

Host-related life history traits in interspecific hybrids of cactophilic Drosophila

In the genus Drosophila (Diptera: Drosophilidae), interspecific hybridization is a rare phenomenon. However, recent evidence suggests a certain degree of introgression between the cactophilic siblings Drosophila buzzatii Patterson & Wheeler and Drosophila koepferae Fontdevila & Wasserman. In this article, we analyzed larval viability and developmental time of hybrids between males of D. buzzatii and females of D. koepferae, raised in media prepared with fermenting tissues of natural host plants that these species utilize in nature as breeding sites. In all cases, developmental time and larval viability in hybrids was not significantly different from parental lines and, depending on the cross, hybrids developed faster than both parental species or than the slowest species. When data of wing length were included in a discriminant function analysis, we observed that both species can be clearly differentiated, while hybrids fell in two categories, one intermediate between parental species and the other consisting of extreme phenotypes. Thus, our results point out that hybrid fitness, as measured by developmental time and viability, is not lower than in the parental species.     

A study of wing morphology and fluctuating asymmetry in interspecific hybrids between Drosophila buzzatii and D. koepferae

In this work we investigate the effect of interspecific hybridization on wing morphology using geometric morphometrics in the cactophilic sibling species D. buzzatii and D. koepferae. Wing morphology in F₁ hybrids exhibited an important degree of phenotypic plasticity and differs significantly from both parental species. However, the pattern of morphological variation between hybrids and the parental strains varied between wing size and wing shape, across rearing media, sexes, and crosses, suggesting a complex genetic architecture underlying divergence in wing morphology. Even though there was significant fluctuating asymmetry for both, wing size and shape in F₁ hybrids and both parental species, there was no evidence of an increased degree of fluctuating asymmetry in hybrids as compared to parental species. These results are interpreted in terms of developmental stability as a function of a balance between levels of heterozygosity and the disruption of coadaptation as an indirect consequence of genomic divergence.     

Consequences of inter-population crosses on developmental stability and canalization of floral traits in Dalechampia scandens (Euphorbiaceae)

Congruence between changes in phenotypic variance and developmental noise in inter-population hybrids was analysed to test whether environmental canalization and developmental stability were controlled by common genetic mechanisms. Developmental stability assessed by the level of fluctuating asymmetry (FA), and canalization by the within- and among-individual variance, were measured on several floral traits of Dalechampia scandens (Euphorbiaceae). Hybridization affected canalization. Both within- and among-individual phenotypic variance decreased in hybrids from populations of intermediate genetic distance, and strongly increased in hybrids from genetically distant populations. Mean-trait FA differed among cross-types, but hybrids were not consistently more or less asymmetric than parental lines across traits. We found no congruence between changes in FA and changes in phenotypic variance. These results suggest that developmental stability (measured by FA) and canalization are independently controlled. This study also confirms the weak relationship between FA and the breakdown of coadapted gene complexes following inter-population hybridization.     

Hybrid disadvantage in the larval foraging behaviour of the two neotropical species of <Emphasis Type="Italic">Drosophila pavani</Emphasis> and <Emphasis Type="Italic">Drosophila gaucha</Emphasis>

Flies from two populations of the Chilean endemic neotropical species Drosophila pavani and two populations of its sibling species Drosophila gaucha were crossed reciprocally to obtain intra- and interspecific hybrids. The developmental pathways of locomotor activity and feeding rate were analysed for eleven of twelve possible genotype groups. The hybrids showed reduced fitness indicated by a decrease in the measured traits. Hybrid disadvantage was strongest in interspecific hybrids, especially with respect to feeding behaviour. This evidence supports the contention that D. pavani and D. gaucha have evolved different coadapted gene pools controlling the developmental pathways for behavioural traits expressed during larval foraging; but genetic divergence affecting these behaviours has also taken place between locally adapted populations within each species.     

Effect of directional selection for body size on fluctuating asymmetry in certain morphological traits in <Emphasis Type="Italic">Drosophila ananassae</Emphasis>

Variation in the subtle differences between the right and left sides of bilateral characters or fluctuating asymmetry (FA) has been considered as an indicator of an organism’s ability to cope with genetic and environmental stresses during development. However, due to inconsistency in the results of empirical studies, the relationship between FA and stress has been the subject of intense debate. In this study, we investigated whether stress caused by artificial bidirectional selection for body size has any effect on the levels of FA of different morphological traits in Drosophila ananassae. The realised heritability (h²) was higher in low-line females and high-line males, which suggests an asymmetrical response to selection for body size. Further, the levels of FA were compared across 10 generations of selection in different selection lines in both sexes for sternopleural bristle number, wing length, wing-to-thorax ratio, sex comb-tooth number and ovariole number. The levels of FA differed significantly among generations and selection lines but did not change markedly with directional selection. However, the levels of FA were higher in the G10 generation (at the end of selection) than G0 (at the start of selection) but lower than the G5 generation in different selection lines, suggesting that the levels of FA are not affected by the inbreeding generated during the course of selection. Also, the levels of FA in the hybrids of high and low lines were significantly lower than the parental selection lines, suggesting that FA is influenced by hybridisation. These results are discussed in the framework of the literature available on FA and its relationship with stress.     

Transgressive character expression in hybrid zones between the native invasives Tithonia tubaeformis and Tithonia rotundifolia (Asteraceae) in Mexico

Natural hybridization frequently promotes gene introgression among closely related species in sympatric populations, producing complex patterns of morphological variation. Therefore, a detailed understanding of the dynamics of interspecific gene flow and its morphological patterns is of widespread interest. We tested if introgressive hybridization promotes an increase in transgressive characters in comparison with the parental species. A sunflower species complex occurring in Mexico formed by two native invasive species, Tithonia tubaeformis and Tithonia rotundifolia, was analyzed using 46 morphological characters (leaf, flower and fruit) in five hybrid zones (N = 150 individuals) and two pure sites for each parental species (N = 80 individuals). In general, T. tubaeformis differed significantly from T. rotundifolia in all the examined characters, except six foliar and one inflorescence character. Morphological characters support the hypothesis of hybridization in this complex, even though both species remain morphological distinct in mixed stands. Individual hybrids appear to be a mosaic of parent-like (24.8 % of traits), intermediate (26.1 %) and transgressive (37.8 %) phenotypes (the remaining 11.3 % of the traits did not differ significantly from both parental species). Our results suggest that individuals from the same parental species were more similar among themselves than to putative hybrids, indicating occasional hybridization with segregation in hybrid types or backcrossing to parents. Evidence indicates a unidirectional pattern of gene flow toward T. rotundifolia.     

Embryonic lethality leads to hybrid male inviability in hybrids between Drosophila melanogaster and D. santomea

The study of the morphological defects unique to interspecific hybrids can reveal which developmental pathways have diverged between species. Drosophila melanogaster and D. santomea diverged more than 10 million years ago, and when crossed produce sterile adult females. Adult hybrid males are absent from all interspecific crosses. We aimed to determine the fate of these hybrid males. To do so, we tracked the development of hybrid females and males using classic genetic markers and techniques. We found that hybrid males die predominantly as embryos with severe segment‐specification defects while a large proportion of hybrid females embryos hatch and survive to adulthood. In particular, we show that most male embryos show a characteristic abdominal ablation phenotype, not observed in either parental species. This suggests that sex‐specific embryonic developmental defects eliminate hybrid males in this interspecific cross. The study of the developmental abnormalities that occur in hybrids can lead to the understanding of cryptic molecular divergence between species sharing a conserved body plan.     

Deficiency mapping of the genomic regions associated with effects on developmental stability in Drosophila melanogaster

Developmental stability is the tendency of morphological traits to resist the effects of developmental noise, and is commonly evaluated by examining fluctuating asymmetry (FA)-random deviations from perfect bilateral symmetry. Molecular mechanisms that control FA have been a long-standing topic of debate in the field of evolutionary biology and quantitative genetics. In this study, we mapped genomic regions associated with effects on the mean and FA of morphological traits, and characterized the trait specificity of those regions. A collection of isogenic deficiency strains established by the DrosDel project was used for deficiency mapping of genome regions associated with effects on FA. We screened 435 genome deficiencies or approximately 64.9% of the entire genome of Drosophila melanogaster to map the region that demonstrated a significant effect on FA of morphological traits. We found that 406 deficiencies significantly affected the mean of morphological traits, and 92 deficiencies increased FA. These results suggest that several genomic regions have the potential to affect developmental stability. They also suggest the possibility of the existence of trait-specific and trait-nonspecific mechanisms for stabilizing developmental processes. The new findings in this study could provide insight into the understanding of the genetic architecture underlying developmental stability.     

FLUCTUATING ASYMMETRY IN A SALIX HYBRID SYSTEM: THE IMPORTANCE OF GENETIC VERSUS ENVIRONMENTAL CAUSES

To examine the effects of hybridization and environmental stress on developmental instability, we examined fluctuating asymmetry (FA), the variance in random deviations from perfect symmetry in bilaterally symmetrical traits, for leaf symmetry in a Salix hybrid system. An abiotic environmental stress (water stress), an interspecific biotic stress (pathogen attack), and an intraspecific biotic stress (competition) were examined to determine which factors increase developmental instability. None of these three environmental stressors significantly increased FA. However, genetic stress through hybridization was detected; hybrid plants showed significantly higher levels of FA than parental species. In contrast to hybridization providing greater developmental stability through heterozygosity, these results suggest that complex, nonadditive interactions provided developmental stability and that developmental instability increased when coadapted gene complexes were disrupted through hybridization. In addition, plant biomass was significantly, negatively correlated with FA, suggesting that those individuals that were more able to buffer themselves against the disruptive effects of environmental stress may have a selective advantage over those that are less able to buffer themselves against these disruptive effects.     

A meristic trait in Drosophila melanogaster x simulans hybrids

A quantitative trait, abdominal bristle number, is described in a number of stocks of the two sibling species Drosophila melanogaster and Drosophila simulans and in interspecific hybrids obtained from these stocks. Coefficients of variation for the trait in the parental species and the hybrids are compared, and in the case of the latter are found to fall in the same range as those of the pure species. The results are discussed in the light of previous findings on other bristle systems.     

Variable modes of inheritance of morphometrical traits in hybrids between Drosophila melanogaster and Drosophila simulans.

We investigated body-size inheritance in interspecific sterile hybrids by crossing a Drosophila simulans strain with 13 strains of Drosophila melanogaster, which were of various origins and chosen for their broad range of genetic variation. A highly significant parent-offspring correlation was observed, showing that the D. melanogaster genes for size are still expressed in a hybrid background. Superimposed on to this additive inheritance, the size of hybrids was always less than the mid-parent value. This phenomenon, which at first sight might be described as dominance or overdominance, is more precisely interpreted as a consequence of a hybrid breakdown, that is, a dysfunction of the parental genes for size when put to work together. This interpretation is enforced by the fact that phenotypic variability was much more prevalent in hybrids than in parents. We also analysed body pigmentation inheritance in the same crosses and got a very different picture. There was no increase in the phenotypic variance of F(1) hybrids and only a low parent-offspring correlation. Apparent overdominance could be observed but in opposite directions, with no evidence of hybrid breakdown. Our data point to the possibility of analysing a diversity of quantitative traits in interspecific hybrids, and indicate that breakdown might be restricted to some traits only.