Patterns of variation in wing morphology in the cactophilic Drosophila buzzatii and its sibling D. koepferae

Drosophila buzzatii and D. koepferae are two sibling species that breed on the necrotic tissues of several cactus species and show a certain degree of niche overlap. Also, they show differences in several life history traits, such as body size and developmental time, which probably evolved as a consequence of adaptation to different host plants. In this work we investigate the ecological and genetic factors affecting wing morphology variation both within and between species. Three wing traits were scored, distal and proximal wing length and width in isofemale lines reared in two of the most important host cacti: Opuntia sulphurea and Trichocereus terschekii. Our results revealed that differences between species and sexes in wing size and shape were significant, whereas the cactus factor was only significant for wing size. Intraspecific analyses showed that differences among isofemale lines were highly significant for both size and shape in both species, suggesting that an important fraction of variation in wing morphology has a genetic basis. Moreover, the line by cactus interaction, which can be interpreted as a genotype by environment interaction, also accounted for a significant proportion of variation. In summary, our study shows that wing size is phenotypically plastic and that populations of D. buzzatii and D. koepferae harbour substantial amounts of genetic variation for wing size and shape. Interspecific differences in wing size and shape are interpreted in terms of spatial predictability of the different host plants in nature.     

Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts

Drosophila koepferae and D. buzzatii are two closely related cactophilic species inhabiting the arid lands of southern South America. Previous studies have shown that D. buzzatii breeds primarily on the necrotic cladodes of several Opuntia cacti and D. koepferae on the rotting stems of columnar cacti of the genera Trichocereus and Cereus. In this paper, we analyze the patterns of host plant utilization in a locality where both Drosophila species are sympatric. Field studies showed an absence of differential attraction of adult flies to the rots of two major host cacti: O. sulphurea and T. terschekii. However, the proportion of D. buzzatii flies emerged from the rotting cladodes of O. sulphurea was significantly higher than in T. terschekii. In laboratory experiments, egg to adult viability in single species cultures varied when both Drosophila species were reared in media prepared with O. sulphurea or T. terschekii. In addition, between-species comparisons of flies emerged from single species cultures showed that D. buzzatii adults were smaller and developed faster than D. koepferae. Furthermore, analysis of flies emerged in mixed species cultures showed differences in oviposition preference and oviposition behavior. We discuss the observed between-species differences and suggest that these traits are the result of adaptation to specific patterns of spatial and temporal predictability of their respective preferred host plants: columnar are less dense and less ephemeral resources, whereas the opuntias are more abundant, and fast rotting cacti. This revised version was published online in July 2006 with corrections to the Cover Date.     

How do similarities in spatial distributions and interspecific associations affect the coexistence of Quercus species in the Baotianman National Nature Reserve,Henan, China

Congeneric species often have similar ecological characteristics and use similar resources. These similarities may make it easier for them to co‐occur in a similar habitat but may also lead to strong competitions that limit their coexistence. Hence, how do similarities in congeneric species affect their coexistence exactly? This study mainly used spatial point pattern analysis in two 1 hm² plots in the Baotianman National Nature Reserve, Henan, China, to compare the similarities in spatial distributions and interspecific associations of Quercus species. Results revealed that Quercus species were all aggregated under the complete spatial randomness null model, and aggregations were weaker under the heterogeneous Poisson process null model in each plot. The interspecific associations of Quercus species to non‐Quercus species were very similar in Plot 1. However, they can be either positive or negative in different plots between the co‐occurring Quercus species. The spatial distributions of congeneric species, interspecific associations with non‐Quercus species, neighborhood richness around species, and species diversity were all different between the two plots. We found that congeneric species did have some similarities, and the closely related congeneric species can positive or negative associate with each other in different plots. The co‐occurring congeneric species may have different survival strategies in different habitats. On the one hand, competition among congenerics may lead to differentiation in resource utilization. On the other hand, their similar interspecific associations can strengthen their competitive ability and promote local exclusion to noncongeneric species to obtain more living space. Our results provide new knowledge for us to better understand the coexistence mechanisms of species.     

Population genetic study of allozyme variation in natural populations of Drosophila antonietae (Insecta, Diptera)

Drosophila antonietae is an endemic South American cactophilic species found in relictual xerophytic vegetation, mostly associated with Cereus hildmaniannus cactus. Low differentiation among populations of this species has been detected using several markers. In this work, we performed an allozyme genetic variability analysis of 11 natural populations of D. antonietae and included a discussion about the possible influences of several evolutionary processes that might be acting to maintain the pattern observed. The genetic variability of 14 isoenzyme loci was analysed and showed a high genetic diversity (average observed heterozygosity = 0.319) and a moderate genetic differentiation among populations ( F statistics = 0.0723). A correlation between genetic and geographical and ecological distances was detected among pairs of populations and the regional equilibrium analysis was thus applied. This analysis resulted in Nm (number of migrants) of approximately 3.21, indicating that moderate levels of both gene flow and genetic drift occur in this species, with gene flow overlapping genetic drift. However, considering ecological features of drosophilids, we propose a hypothesis to explain the moderate differentiation encountered as a result of three different processes, or a combination of them: (1) gene flow; (2) a short period of differentiation, i.e. maintenance of ancestral polymorphism; and (3) action of natural selection. Moreover, if gene flow is present, the high genetic diversity compared with other cactophilic and non-cactophilic species could be due to differential selection in different populations followed by gene exchange among them. These factors are discussed in the light of D. antonietae 's historical and evolutionary association with the host cactus.     

Estimation of migration from a perturbation experiment in natural populations of Drosophila buzzatii Patterson & Wheeler

In order to estimate migration and gene flow, allele frequencies in populations at two sites separated by 120 m were differentially perturbed by the continuous release over 413 days of flies homozygous at particular allozyme loci. The effects of perturbation were determined by genotype assay at two collections prior to, thirteen during and nine after the perturbation period. Maximum likelihood methods were developed to estimate migration into the two populations from the homozygous releases, and migration between the two populations. The successful perturbation of allele frequencies in a natural population is demonstrated. A plateau in allele frequencies during perturbation and a return to original frequencies following cessation of perturbation was most likely due to selection during development against recessive alleles concurrently introduced into the populations by the released flies. There is unequivocal evidence for short distance gene flow between the two populations. The migration rates estimated at ten times over a nine month period were extremely variable, but with higher population density at one site positively related with migration from that site to the other.     

Coexistence of ecologically similar colonising species III. Drosophila aldrichi and D. buzzatii: larval performance on,and adult preference for,three Opuntia cactus species

Two Drosophila species, D. buzzatti and D. aldrichi, coexist on several species of Opuntia cacti in Australia, primarily on O. tomentosa and O. streptacantha in the northern part of the cactus distribution, and on O. stricta in the south. Thorax length of field-collected adults was less, and the variance in length greater, than that for flies reared on simulated rots in the laboratory, indicating that these species are affected by crowding in nature. A larval performance index, measured on simulated cactus rots at low, moderate and high densities in single-species cultures, and at moderate and high densities in mixed-species cultures, was used to compare the relative intensity of intra- and interspecific competition at the same total larval density per 5 g necrotic cactus. Larval performance of both fly species was greatest on O. streptacantha, intermediate on O. tomentosa, and least on O. stricta in both single-species and mixed-species cultures. On O. stricta, the performances of D. aldrichi and D. buzzatii were not different when in single-species cultures, but that of D. aldrichi decreased significantly in mixed-species cultures. On the other two cactus species, the performances of D. aldrichi and D. buzzattii were not different in mixed-species cultures. The order of preferences by adult females for the cacti differed from that for larval performance, with females of both species prefering O. stricta. Analysis of microbial numbers growing on the cacti showed little difference among cacti at the rot age used for testing adult preference, but later growth was greater on O. tomentosa and O. streptacantha, the cacti that best supported larvae. Differential larval performance on O. stricta may contribute to the rare presence of D. aldrichi in the southern part of the cactus distribution, while the superior quality of O. tomentosa and O. streptacantha (larger rot size and higher microbial concentration) may reduce competition and facilitate cocxistence of the fly species in the north.     

Genetic variation and plasticity of thorax length and wing length in Drosophila aldrichi and D. buzzatii

Reaction norms across three temperatures of development were measured for thorax length, wing length and wing length/thorax length ratio for ten isofemale lines from each of two populations of Drosophila aldrichi and D. buzzatii. Means for thorax and wing length in both species were larger at 24 °C than at either 18 °C or 31 °C, with the reduction in size at 18 °C most likely due to a nutritional constraint. Although females were larger than males, the sexes were not different for wing length/thorax length ratio. The plasticity of the traits differed between species and between populations of each species, with genetic variation in plasticity similar for the two species from one locality, but much higher for D. aldrichi from the other. Estimates of heritabilities for D. aldrichi generally were higher at 18 °C and 24 °C than at 31 °C, but for D. buzzatii they were highest at 31 °C, although heritabilities were not significantly different between species at any temperature. Additive genetic variances for D. aldrichi showed trends similar to that for heritability, being highest at 18 °C and decreasing as temperature increased. For D. buzzatii, however, additive genetic variances were lowest at 24 °C. These results are suggestive that genetic variation for body size characters is increased in more stressful environments. Thorax and wing lengths showed significant genetic correlations that were not different between the species, but the genetic correlations between each of these traits and their ratio were significantly different. For D. aldrichi, genetic variation in the wing length/thorax length ratio was due primarily to variation in thorax length, while for D. buzzatii, it was due primarily to variation in wing length. The wing length/thorax length ratio, which is the inverse of wing loading, decreased linearly as temperature increased, and it is suggested that this ratio may be of greater adaptive significance than either of its components.     

Do rabbits eat voles? Apparent competition,habitat heterogeneity and large‐scale coexistence under mink predation

Habitat heterogeneity is predicted to profoundly influence the dynamics of indirect interspecific interactions; however, despite potentially significant consequences for multi-species persistence, this remains almost completely unexplored in large-scale natural landscapes. Moreover, how spatial habitat heterogeneity affects the persistence of interacting invasive and native species is also poorly understood. Here we show how the persistence of a native prey (water vole, Arvicola terrestris ) is determined by the spatial distribution of an invasive prey (European rabbit, Oryctolagus cuniculus ) and directly infer how this is defined by the mobility of a shared invasive predator (American mink, Neovison vison ). This study uniquely demonstrates that variation in habitat connectivity in large-scale natural landscapes creates spatial asynchrony, enabling coexistence between apparent competitive native and invasive species. These findings highlight that unexpected interactions may be involved in species declines, and also that in such cases habitat heterogeneity should be considered in wildlife management decisions.     

Phenotypic plasticity in Drosophila cactophilic species: the effect of competition,density, and breeding sites

Changes in the environmental conditions experienced by naturally occurring populations are frequently accompanied by changes in adaptive traits allowing the organism to cope with environmental unpredictability. Phenotypic plasticity is a major aspect of adaptation and it has been involved in population dynamics of interacting species. In this study, phenotypic plasticity (i.e., environmental sensitivity) of morphological adaptive traits were analyzed in the cactophilic species Drosophila buzzatii and Drosophila koepferae (Diptera: Drosophilidae) considering the effect of crowding conditions (low and high density), type of competition (intraspecific and interspecific competition) and cacti hosts (Opuntia and Columnar cacti). All traits (wing length, wing width, thorax length, wing loading and wing aspect) showed significant variation for each environmental factor considered in both Drosophila species. The phenotypic plasticity pattern observed for each trait was different within and between these cactophilic Drosophila species depending on the environmental factor analyzed suggesting that body size‐related traits respond almost independently to environmental heterogeneity. The effects of ecological factors analyzed in this study are discussed in order to elucidate the causal factors investigated (type of competition, crowding conditions and alternative host) affecting the election of the breeding site and/or the range of distribution of these cactophilic species.     

Genetic history of a colonizing population: Drosophila buzzatii (Diptera: Drosophilidae) in Australia

Drosophila buzzatii Patterson & Wheeler, a cactophilic species that feeds and breeds in the rotting tissues of various Opuntia cactus species, was inadvertently introduced to Australia from Argentina sometime during the period 1931–1936. After a bottleneck at introduction, its spread through the cactus distribution was probably very rapid as a result of natural dispersal from the site of introduction and from three other foci colonized from the introduction site by human intervention. By 1940, the Opuntia distribution and consequently that of D. buzzatii was reduced to spatially isolated populations, with probable further bottlenecking of at least some of the D. buzzatii populations. Allozyme data (primarily six polymorphic loci) from flies collected during April 1972 to February 1996 at 67 localities were used to examine current population differentiation and relationships, as well as to infer aspects of their demographic history. Although there is significant isolation‐by‐distance, genetic relationships among the populations are not simply related to geographical distance, implying that genetic drift has contributed to population differentiation. However, the biotic and, to an extent, the physical environment are not the same in Australia as in Argentina. Consequently, exposure to novel environments has led to local adaptation and further population differentiation. Genetic variation and the structure of Australian populations apparently are determined by founder effects (drift) at the level of individual breeding sites (cactus rots), by diversifying selection among rots within a locality, as well as by drift and geographically varying selection among localities. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2013, 109 , 682–698.     

Competitive interactions and persistence of two nematode species that parasitize Drosophila recens

Drosophila recens is parasitized in the wild by two nematodes, Howardula aoronymphium , a host generalist, and Parasitylenchus nearcticus , a host specialist known only from D .  recens . In order to understand how these two parasite species coexist, we compared their ability to infect and grow in D .  recens , their effects on host fecundity and survival, and whether one parasite species was competitively superior in double infections. The specialist nematode P. nearcticus had greater rates of infection and reproduction than the generalist H. aoronymphium , and completely sterilized females in single and mixed infections. The specialist was competitively superior in mixed infections, as generalist motherworms were significantly smaller than in single infections. These results suggest that P. nearcticus might competitively exclude H. aoronymphium if D. recens were the only host available. It is likely that H. aoronymphium persists in D. recens by transmission from other, more suitable host species.     

Marine sponges of the Dampier Archipelago, Western Australia: patterns of species distributions, abundance and diversity

Quantitative surveys revealed high diversity (species richness) of sponges (150 species) in the previously little explored Dampier Archipelago, northwestern Australia. Classification analyses disclosed 11 station groups with high internal heterogeneity in species composition, however some spatial patterns were evident. The composition of sponge assemblages varied with environmental factors such as substrate type (coral, igneous rock, limestone rock), aspect (exposed, protected), substrate configuration (limestone platform, dissected reef) and depth. Most of the species (61%) reported from the Dampier Archipelago were rare (found at one or two stations). The number of species found at only one location was high (48%), supporting previous findings that northwestern Australia has high sponge endemism. As a result of all sponge surveys undertaken in the archipelago (qualitative and quantitative, subtidal and intertidal), 275 sponge species have now been reported from the area. This number indicates high species diversity in the region. Estimations of diversity based on non-parametric modelling suggests that there are potentially more species (range 245–346) than presently recorded in the archipelago.     

Remating and sperm displacement in a natural population of Drosophila buzzatii inferred from mother-offspring analysis of microsatellite loci

Prospects for estimation of parameters of models of sperm competition from field data have improved recently with the development of methods that employ multilocus genotype data from brood-structured samples. Sperm competition in Drosophila buzzatii is of special interest because it is possible to directly observe the breeding behaviour of this species in its natural habitat of rotting cactus. Previous laboratory experiments showed that this species exhibits an unusual pattern of frequent remating and sperm partitioning. This paper reports the first attempt to estimate the frequency of female remating and sperm competition in natural populations of D. buzzatii. For the Australian population studied, the mean remating frequency was lower (alpha = 2.12-2.20) than previously estimated in laboratory experiments with the same population, whereas mean sperm displacement (beta = 0.69-0.71) fell within the limits of previous laboratory results. The evolution of the D. buzzatii mating system is discussed.     

Ecology of body size in Drosophila buzzatii: untangling the effects of temperature and nutrition

Abstract.

• 1 A method of separating the effects of two important determinants of body size in natural populations, temperature of larval development and level of larval nutrition, by making measurements of thorax length and wing length of adult flies is investigated.
• 2 I show that at any given time variation in body size of Drosophila buzzatii from two sites in eastern Australia is determined primarily by variation in the quality of nutrition available to larvae.
• 3 Throughout the year adult flies are consistently at least 25% smaller in volume than predicted for optimal nutrition at their predicted temperature of larval development.
• 4 Nutritional stress is therefore a year-round problem for these flies.
• 5 Measurements of adult flies emerging from individual breeding substrates (rotting cactus cladodes) show that there is substantial variation among these substrates in the nutrition available to larvae.
• 6 This method will allow study of spatial and temporal variation in the temperature of larval substrates and in the nutritional resources available to flies in natural populations.

     

Geographical variation in resistance of the parasitoid Asobara tabids against encapsulation by Drosophila melanoqaster larvae: the mechanism explored

Abstract. The braconid parasitoid Asobara tabida Nees attacks larvae of several Drosophila species in fermenting substrates. Northwestern and central European populations of the parasitoid attack mainly D.subobscura Collin. Southern European parasitoids attack mainly D.melanogaster Meigen. Larvae of this last species can defend themselves against parasitoids by encapsulating the parasitoid egg. Parasitoids from southern European populations are better able to resist encapsulation of their eggs than their northwestern and central European conspecifics. The eggs of southern European parasitoids appear to have a 'sticky' egg chorion. As a result of this 'stickiness' the eggs become embedded in host tissue where they are not completely covered by the host's blood cells. This leads to, at most, partial encapsulation of the egg. Parasitoid larvae can escape from partially closed capsules.     

Retired flies,hidden plateaus,and the evolution of senescence in Drosophila melanogaster

Late‐life plateaus in age‐specific mortality have been an evolutionary and biodemographic puzzle for decades. Although classic theory on the evolution of senescence predicts late‐life walls of death, observations in experimental organisms document the opposite trend: a slowing in the rate of increase of mortality at advanced ages. Here, I analyze published life‐history data on individual Drosophila melanogaster females and argue for a fundamental change in our understanding of mortality in this important model system. Mortality plateaus are not, as widely assumed, exclusive to late life, and are not explained by population heterogeneity—they are intimately connected to individual fecundity. Female flies begin adult life in the working stage, a period of active oviposition and low but accelerating mortality. Later they transition to the retired stage, a terminal period characterized by limited fecundity and relatively constant mortality. Because ages of transition differ between flies, age‐synchronized cohorts contain a mix of working and retired flies. Early‐ and mid‐life plateaus are obscured by the presence of working flies, but can be detected when cohorts are stratified by retirement status. Stage‐specificity may be an important component of Drosophila life‐history evolution.     

Genetic and phenotypic correlations among size-related traits, and heritability variation between body parts in Drosophila buzzatii

Recent studies have shown that body size is a heritable trait phenotypically correlated with several fitness components in wild populations of the cactophilic fly Drosophila buzzatii. To obtain further information on size-related variation, heritabilities as well as genetic and phenotypic correlations among size-related traits of several body parts (head, thorax and wings) were estimated. The study was carried out on an Argentinean natural population in which size-related selection was previously detected. The genetic parameters were estimated using offspring-parent regressions (105 families) in the laboratory G₂ generation of a sample of wild flies. The traits were also scored in Wild-Caught Flies (WCF). Laboratory-Reared Flies (LRF) were larger and less variable than WCF. Although heritability estimates were significant for all traits, heritabilities were higher for thorax-wing traits than for head traits. Phenotypic and genetic correlations were all positive. The highest genetic correlations were found between traits which are both functionally and developmentally related. Genetic and phenotypic correlations estimated in the lab show similar correlation patterns (r = 0.49; TP = 0.02, Mantel's test). However, phenotypic correlations were found to be typically larger in WCF than in LRF. The genetic correlation matrix estimated in the relatively homogeneous lab environment is not simply a constant multiplicative factor of the phenotypic correlation matrix estimated in WCF. This revised version was published online in July 2006 with corrections to the Cover Date.     

The abundance and geographic distributions of two species of ticks in South Australia: Bundey Bore revisited

Perhaps one of the central questions in ecology has been what limits the geographic distribution of species. The geographic distributions of the reptile-ticks Amblyomma limbatum, Bothriocroton hydrosauri and Amblyomma albolimbatum are a classic example of this problem: where these ticks meet, narrow regions-of-overlap often occur. Despite studies of interactions among these ticks, and of these ticks and their environment, we still do not understand what limits their geographic distributions. Many hypotheses have been proposed and tested, but all have seemingly been rejected. Our aim was to account for the abundance and the geographic distributions of A. limbatum and B. hydrosauri at Bundey Bore Station, South Australia, where these species come in contact and have been studied for over 35 years, leading to over 55 000 records of reptiles and their ticks using a capture-mark-recapture approach. We constructed models which had combinations of temperature and moisture indices from different months of the year to determine the relationship between climate and tick abundance, and between climate and the shifting local geographic distribution of A. limbatum and B. hydrosauri at Bundey Bore Station. We found that climate together with the abundance of ticks in the previous year and the abundance of the lizard host, accounted for 54%–77% of the variation in the abundance of A. limbatum and B. hydrosauri among years. We also found that the climate in late autumn to winter, together with the abundance of ticks and their host, accounted for 18%–84% of the variation in the geographic distributions of these ticks among years. Climate was central to the abundance and the geographic distributions of A. limbatum and B. hydrosauri at Bundey Bore Station. We speculate that the same mechanisms account for the geographic distributions of A. limbatum, B. hydrosauri and A. albolimbatum elsewhere in Australia; so, climate may explain the three-tick problem in Austral ecology.