Carla Rego

SYMMETRY BREAKING IN INTERSPECIFIC DROSOPHILA HYBRIDS IS NOT DUE TO DEVELOPMENTAL NOISE

Abstract 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 covariation 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.

CLINAL PATTERNS OF CHROMOSOMAL INVERSION POLYMORPHISMS IN DROSOPHILA SUBOBSCURA ARE PARTLY ASSOCIATED WITH THERMAL PREFERENCES AND HEAT STRESS RESISTANCE

Latitudinal clines in the frequency of various chromosomal inversions are well documented in Drosophila subobscura. Because these clines are roughly parallel on three continents, they have undoubtedly evolved by natural selection. Here, we address whether individuals carrying different chromosomal arrangements also vary in their thermal preferences (Tp) and heat stress tolerance (Tko). Our results show that although Tp and Tko were uncorrelated, flies carrying “cold‐adapted” gene arrangements tended to choose lower temperatures in the laboratory or had a lower heat stress tolerance, in line with what could be expected from the natural patterns. Different chromosomes were mainly responsible for the underlying genetic variation in both traits, which explains why they are linearly independent. Assuming Tp corresponds closely with temperatures that maximize fitness our results are consistent with previous laboratory natural selection experiments showing that thermal optimum diverged among thermal lines, and that chromosomes correlated with Tp differences responded to selection as predicted here. Also consistent with data from the regular tracking of the inversion polymorphism since the colonization of the Americas by D. subobscura, we tentatively conclude that selection on tolerance to thermal extremes is more important in the evolution and dynamics of clinal patterns than the relatively “minor” adjustments from behavioral thermoregulation.

Hsp70 protein levels and thermotolerance in Drosophila subobscura: A reassessment of the thermal co-adaptation hypothesis

Theory predicts that geographic variation in traits and genes associated with climatic adaptation may be initially driven by the correlated evolution of thermal preference and thermal sensitivity. This assumes that an organism’s preferred body temperature corresponds with the thermal optimum in which performance is maximized; hence, shifts in thermal preferences affect the subsequent evolution of thermal‐related traits. Drosophila subobscura evolved worldwide latitudinal clines in several traits including chromosome inversion frequencies, with some polymorphic inversions being apparently associated with thermal preference and thermal tolerance. Here we show that flies carrying the warm‐climate chromosome arrangement O3+4 have higher basal protein levels of Hsp70 than their cold‐climate Ost counterparts, but this difference disappears after heat hardening. O3+4 carriers are also more heat tolerant, although it is difficult to conclude from our results that this is causally linked to their higher basal levels of Hsp70. The observed patterns are consistent with the thermal co‐adaptation hypothesis and suggest that the interplay between behaviour and physiology underlies latitudinal and seasonal shifts in inversion frequencies.

CONVERGENCE TO A NOVEL ENVIRONMENT: COMPARATIVE METHOD VERSUS EXPERIMENTAL EVOLUTION

Abstract Laboratory adaptation allows researchers to contrast temporal studies of experimental evolution with comparative studies. The comparative method is here taken to mean the inference of microevolutionary processes from comparisons among contemporaneous populations of diverse origins, from one or multiple species. The data contrasted here come from Drosophila subobscura populations that were introduced to the laboratory at several different times and from two different locations. Two questions were addressed. First, can we correctly infer evolutionary dynamics from comparative data collected simultaneously from disparate populations? In most cases, we could, except for the character of starvation resistance. Second, are the evolutionary dynamics inferred from the comparative approach similar to those revealed by temporal studies of experimental evolution? For fecundity characters, they were. Overall the results show that both comparative and temporal studies are useful, though the former can be uninformative for characters with complex evolutionary trajectories.

An evolutionary no man’s land

The gap between evolutionary studies in laboratory versus natural populations is a persistent problem1xSee all References, 2xLaboratory selection experiments using Drosophila: what do they really tell us?. Harshman, L.G. and Hoffmann, A.A. Trends Ecol. Evol. 200; 15: 32–36See all References. In an attempt to bridge this gap, some researchers in the early 1980s studied the quantitative genetics of laboratory populations recently founded from the wild, with and without inbreeding3xSee all References, 4xGenetic correlation structure of life history variables in outbred, wild Drosophila melanogaster: effects of photoperiod regimen. Giesel, J.T. Am. Nat. 1986; 128: 593–603CrossrefSee all References. The dangers of such approaches were soon demonstrated experimentally5xGenetic covariation in Drosophila life history: untangling the data. Rose, M.R. Am. Nat. 1984; 123: 565–569CrossrefSee all References, 6xGenetic covariation among life-history components: the effect of novel environments. Service, P.M. and Rose, M.R. Evolution. 1985; 39: 943–945CrossrefSee all References. Inbreeding depression and genotype-by-environment interactions make such studies unreliable guides to the evolution of populations long-established in any environment. This conclusion is reiterated to some extent in Harshman and Hoffmann’s recent TREE perspective2xLaboratory selection experiments using Drosophila: what do they really tell us?. Harshman, L.G. and Hoffmann, A.A. Trends Ecol. Evol. 200; 15: 32–36See all References2, where the authors state that, ‘The nature of laboratory selection regimes is unnatural.’ But, they then go on to propose complementing selection experiments in long-established laboratory populations with selection experiments in recently introduced ones. It is not clear how one could disentangle the causes of possible differences from the results of such disparate studies. Furthermore, from first principles and extant experimental studies, we expect a conflation of evolutionary effects in the recently introduced populations because of adaptation to the laboratory environment, and because of genetic and evolutionary disequilibrium. In particular, interactions between adaptation to the general laboratory environment and any particular selective regime under study could be a source of unresolvable evolutionary outcomes, as we will now explain.Two evolutionary processes are at work in the transition from the wild to the laboratory. First, placing a population in a novel environment can cause a change in genetic variances and covariances between traits, as a result of genotype-by-environment interactions. Second, continued maintenance in this novel environment might bring about evolutionary change, perhaps because of new selection pressures or changes in breeding structure. A recently founded laboratory population will thus be in a ‘no man’s land’. We cannot use it to provide information about the original wild population, nor can we test evolutionary models that rely on the assumption that the newly transplanted population is near genetic or selective equilibrium. Surprisingly, like Harshman and Hoffmann, several recent studies have essentially repeated these mistakes7xFluctuating asymmetry, body size and sexual selection in the dung fly Sepsis cynipsea – testing the good genes assumptions and predictions. Blanckenhorn, W.U. et al. J. Evol. Biol. 1998; 11: 735–753Crossref | Scopus (59)See all References, 8xQuantitative genetics of the dung fly Sepsis cynipsea: Cheverud’s conjecture revisited. Reusch, T. and Blanckenhorn, W.U. Heredity. 1998; 81: 111–119CrossrefSee all References, 9xTrade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)?. Windig, J.J. Heredity. 1999; 82: 57–68CrossrefSee all References.Let us conclude with an example. The empirical challenge posed by the transition from wild to laboratory conditions led us to study the evolution of a newly founded laboratory population of Drosophila subobscura10xAdaptation to the laboratory environment in Drosophila subobscura. Matos, M. et al. J. Evol. Biol. 2000; 13: 9–19Crossref | Scopus (48)See all References10. We found that adaptation to the novel, laboratory environment occurred at a relatively fast rate. As an illustration, fecundity around the age of reproduction increased steadily in the generations after establishment in the laboratory, showing convergence to the values of a long-established population serving as a control (maintained in the lab for 24 generations before the foundation of the new one); the fecundity of the new population became similar to that of the long-established population after just 14 generations of adaptation to the laboratory. In this no man’s land between the wild and the laboratory, the population evolved extremely rapidly. Instead of straining for dubious interpretations of the uncertain results afforded by studies of recently sampled populations, we might use the gap between the wild and the laboratory as an evolutionary tool – recognizing that, after all, the lab is just another environment to which populations adapt, albeit a very peculiar one10xAdaptation to the laboratory environment in Drosophila subobscura. Matos, M. et al. J. Evol. Biol. 2000; 13: 9–19Crossref | Scopus (48)See all References10. To this extent, we can agree with Harshman and Hoffmann.

Spatial Factors Play a Major Role as Determinants of Endemic Ground Beetle Beta Diversity of Madeira Island Laurisilva

The development in recent years of new beta diversity analytical approaches highlighted valuable information on the different processes structuring ecological communities. A crucial development for the understanding of beta diversity patterns was also its differentiation in two components: species turnover and richness differences. In this study, we evaluate beta diversity patterns of ground beetles from 26 sites in Madeira Island distributed throughout Laurisilva – a relict forest restricted to the Macaronesian archipelagos. We assess how the two components of ground beetle beta diversity (βrepl – species turnover and βrich - species richness differences) relate with differences in climate, geography, landscape composition matrix, woody plant species richness and soil characteristics and the relative importance of the effects of these variables at different spatial scales. We sampled 1025 specimens from 31 species, most of which are endemic to Madeira Island. A spatially explicit analysis was used to evaluate the contribution of pure environmental, pure spatial and environmental spatially structured effects on variation in ground beetle species richness and composition. Variation partitioning showed that 31.9% of species turnover (βrepl) and 40.7% of species richness variation (βrich) could be explained by the environmental and spatial variables. However, different environmental variables controlled the two types of beta diversity: βrepl was influenced by climate, disturbance and soil organic matter content whilst βrich was controlled by altitude and slope. Furthermore, spatial variables, represented through Moran’s eigenvector maps, played a significant role in explaining both βrepl and βrich, suggesting that both dispersal ability and Madeira Island complex orography are crucial for the understanding of beta diversity patterns in this group of beetles.

Contrasting patterns of phenotypic variation linked to chromosomal inversions in native and colonizing populations of Drosophila subobscura

In fewer than two decades after invading the Americas, the fly Drosophila subobscura evolved latitudinal clines for chromosomal inversion frequencies and wing size that are parallel to the long‐standing ones in native Palearctic populations. By sharp contrast, wing shape clines also evolved in the New World, but the relationship with latitude was opposite to that in the Old World. Previous work has suggested that wing trait differences among individuals are partially due to the association between chromosomal inversions and particular alleles which influence the trait under consideration. Furthermore, it is well documented that a few number of effective individuals founded the New World populations, which might have modified the biometrical effect of inversions on quantitative traits. Here we evaluate the relative contribution of chromosomal inversion clines in shaping the parallel clines in wing size and contrasting clines in wing shape in native and colonizing populations of the species. Our results reveal that inversion‐size and inversion‐shape associations in native and colonizing (South America) populations are generally different, probably due to the bottleneck effect. Contingent, unpredictable evolution was suggested as an explanation for the different details involved in the otherwise parallel wing size clines between Old and New World populations of D. subobscura. We challenge this assertion and conclude that contrasting wing shape clines came out as a correlated response of inversion clines that might have been predicted considering the genetic background of colonizers.

Quantitative genetics of speciation: additive and non-additive genetic differentiation between Drosophila madeirensis and Drosophila subobscura

The role of dominance and epistasis in population divergence has been an issue of much debate ever since the neoDarwinian synthesis. One of the best ways to dissect the several genetic components affecting the genetic architecture of populations is line cross analysis. Here we present a study comparing generation means of several life history-traits in two closely related Drosophila species: Drosophila subobscura, D. madeirensis as well as their F1 and F2 hybrids. This study aims to determine the relative contributions of additive and non-additive genetic parameters to the differentiation of life-history traits between these two species. The results indicate that both negative dominance and epistatic effects are very important in the differentiation of most traits. We end with considerations about the relevance of these findings for the understanding of the role of non-additive effects in speciation.

Seed production and pre-dispersal reproductive losses in the narrow endemic Euphorbia pedroi (Euphorbiaceae)

Euphorbia pedroi is a narrow endemic species with three known populations located in coastal areas of western Portugal. This study focused on the reproductive biology of this species from flowering to dispersal, aiming to identify the factors causing decrease in seed production potential and to assess the spatio-temporal patterns of seed production at the individual and population levels. The abortion of reproductive structures, particularly seeds, represented a major fraction of losses in the potential seed production of E. pedroi. Moth larvae destroyed a variable proportion of cyathia in a large number of plants from the two populations regardless of their degree of isolation. Furthermore, generalist and specialist pre-dispersal seed predators were responsible for temporally variable seed losses unrelated with variables indicative of plant size and fecundity, and showing no consistency at the individual level. Specialist seed-wasps inflicted the highest losses to E. pedroi and their impact was intimately associated with the magnitude of yearly variation in seed production. This finding highlights the role of the inter-annual variation in seed production as a key feature in this plant-seed predator system. The effect of the two groups of seed predators on the reproductive output of E. pedroi was additive and those insects do not seem to exert an important selective pressure on the traits studied. The proportion of intact seeds produced by E. pedroi differed between locations, but not between individuals within each population, highlighting the major contribution of larger plants to the seed pool.

Do Species Converge during Adaptation? A Case Study in Drosophila

Adaptation to novel environments is a crucial theme in evolutionary biology, particularly because ex situ conservation forces populations to adapt to captivity. Here we analyze the evolution of life‐history traits in two closely related species, Drosophila subobscura Collin and Drosophila madeirensis Monclús, during adaptation to the laboratory. Drosophila madeirensis, an endemic species from Madeira, is here shown to have less ability to adapt to the laboratory. Early fecundity was the only trait where this species showed a significant improvement with time. By comparison, D. subobscura improved in most traits, and its early fecundity increased faster than that of D. madeirensis. Our findings suggest that different species, even closely related ones, may adapt at different rates to the same environment.