Species Of Repleta Group Research Articles

Drosophila (Diptera: Drosophilidae) survey in an ‘island’ of xerophytic vegetation within the Atlantic Forest biome, with emphasis on the repleta species group

ABSTRACTThis work performed a seasonal and spatial survey of Drosophila groups, focusing on the repleta group species, in an enclave of xerophytic vegetation in the Araucaria forest phytophysiognomy. The Drosophilidae community, in terms of Drosophila groups, was seasonally affected probably because of cold winters of the highland Araucaria forest surveyed. The spatial variation of groups was not significant, but distinct distributions were observed, both in height and related to the fragment edge/interior, for some groups. Regarding the repleta group, no clear pattern of species seasonal and spatial distribution was detected, probably due to the observation that some species were collected in different seasons and occupied different regions of the area. The considerably high abundance of D. senei, compared to other studies, is one aspect that should be better investigated.

Ectoparasitic mites and their Drosophila hosts

ABSTRACTOnly two parasite interactions are known for Drosophila to date: Allantonematid nematodes associated with mycophagous Drosophilids and the ectoparasitic mite Macrocheles subbadius with the Sonoran Desert endemic Drosophila nigrospiracula. Unlike the nematode-Drosophila association, breadth of mite parasitism on Drosophila species is unknown. As M. subbadius is a generalist, parasitism of additional Drosophilids is expected. We determined the extent and distribution of mite parasitism in nature Drosophilids collected in Mexico and southern California. Thirteen additional species of Drosophilids were infested. Interestingly, 10 belong to the repleta species group of the subgenus Drosophila, despite the fact that the majority of flies collected were of the subgenus Sophophora. In all cases but 2, the associated mites were M. subbadius. Drosophila hexastigma was found to have not only M. subbadius, but another Mesostigmatid mite, Paragarmania bakeri, as well. One D. hydei was also found to have a mite from genus Lasioseius attached. In both choice and no-choice experiments, mites were more attracted to repleta group species than to Sophophoran. The extent of mite parasitism clearly is much broader than previously reported and suggests a host bias mediated either by mite preference and/or some mechanism of resistance in particular Drosophilid lineages.

Radiation of the Drosophila nannoptera species group in Mexico.

The Drosophila nannoptera species group, a taxon of Mexican cactophilic flies, is an excellent model system to study the influence of abiotic and biotic factors on speciation, the genetic causes of ecological specialization and the evolution of unusual reproductive characters. However, the phylogenetic relationships in the nannoptera species group and its position within the virilis-repleta phylogeny have not been thoroughly investigated. Using a multilocus data set of gene coding regions of eight nuclear and three mitochondrial genes, we found that the four described nannoptera group species diverged rapidly, with very short internodes between divergence events. Phylogenetic analysis of repleta group lineages revealed that D.inca and D.canalinea are sister to all other repleta group species, whereas the annulimana species D.aracataca and D.pseudotalamancana are sister to the nannoptera and bromeliae species groups. Our divergence time estimates suggest that the nannoptera species group radiated following important geological events in Central America. Our results indicate that a single evolutionary transition to asymmetric genitalia and to unusual sperm storage may have occurred during evolution of the nannoptera group.

Monophyly, divergence times, and evolution of host plant use inferred from a revised phylogeny of the Drosophila repleta species group

We present a revised molecular phylogeny of the Drosophila repleta group including 62 repleta group taxa and nine outgroup species based on four mitochondrial and six nuclear DNA sequence fragments. With ca. 100 species endemic to the New World, the repleta species group represents one of the major species radiations in the genus Drosophila. Most repleta group species are associated with cacti in arid or semiarid regions. Contrary to previous results, maximum likelihood and Bayesian phylogenies of the 10-gene dataset strongly support the monophyly of the repleta group. Several previously described subdivisions in the group were also recovered, despite poorly resolved relationships between these clades. Divergence time estimates suggested that the repleta group split from its sister group about 21millionyears ago (Mya), although diversification of the crown group began ca. 16Mya. Character mapping of patterns of host plant use showed that flat leaf Opuntia use is common throughout the phylogeny and that shifts in host use from Opuntia to the more chemically complex columnar cacti occurred several times independently during the history of this group. Although some species retained the use of Opuntia after acquiring the use of columnar cacti, there were multiple, phylogenetically independent instances of columnar cactus specialization with loss of Opuntia as a host. Concordant with our proposed timing of host use shifts, these dates are consistent with the suggested times when the Opuntioideae originated in South America. We discuss the generally accepted South American origin of the repleta group.

Molecular weight estimation of esterase isoenzymes in closely related Drosophila Species (Diptera: Drosophilidae) in non-denaturing polyacrylamide gel electrophoresis

A method that allows the measure of molecular weight of two well-known and closely related esterases from Drosophila mojavensis and its sibling species, D. arizonae, is here described, using native polyacrylamide gel electrophoresis at several concentrations, applying Fergunson´s principles. These enzymes, namely EST-4 and EST-5, presented molecular weight values between 81 and 91 kDa. In spite of their distinct expression pattern through the insect's life cycle, they showed properties of isoenzymes codified by distinct structural genes, supporting the hypothesis of a rather recent gene duplication event that generated both in D. mojavensis and D. arizonae, as well as in other species of repleta group. The method is simple and adequate to be applied to preliminary molecular weight determination of other enzymes without any previous purification procedure.

Adaptive Evolution of Recently Duplicated Accessory Gland Protein Genes in Desert Drosophila

The relationship between animal mating system variation and patterns of protein polymorphism and divergence is poorly understood. Drosophila provides an excellent system for addressing this issue, as there is abundant interspecific mating system variation. For example, compared to D. melanogaster subgroup species, repleta group species have higher remating rates, delayed sexual maturity, and several other interesting differences. We previously showed that accessory gland protein genes (Acp's) of Drosophila mojavensis and D. arizonae evolve more rapidly than Acp's in the D. melanogaster subgroup and that adaptive Acp protein evolution is likely more common in D. mojavensis/D. arizonae than in D. melanogaster/D. simulans. These findings are consistent with the idea that greater postcopulatory selection results in more adaptive evolution of seminal fluid proteins in the repleta group flies. Here we report another interesting evolutionary difference between the repleta group and the D. melanogaster subgroup Acp's. Acp gene duplications are present in D. melanogaster, but their high sequence divergence indicates that the fixation rate of duplicated Acp's has been low in this lineage. Here we report that D. mojavensis and D. arizonae genomes contain several very young duplicated Acp's and that these Acp's have experienced very rapid, adaptive protein divergence. We propose that rapid remating of female desert Drosophila generates selection for continuous diversification of the male Acp complement to improve male fertilization potential. Thus, mating system variation may be associated with adaptive protein divergence as well as with duplication of Acp's in Drosophila.

Gene Duplication and Adaptive Evolution of Digestive Proteases in Drosophila arizonae Female Reproductive Tracts

It frequently has been postulated that intersexual coevolution between the male ejaculate and the female reproductive tract is a driving force in the rapid evolution of reproductive proteins. The dearth of research on female tracts, however, presents a major obstacle to empirical tests of this hypothesis. Here, we employ a comparative EST approach to identify 241 candidate female reproductive proteins in Drosophila arizonae, a repleta group species in which physiological ejaculate–female coevolution has been documented. Thirty-one of these proteins exhibit elevated amino acid substitution rates, making them candidates for molecular coevolution with the male ejaculate. Strikingly, we also discovered 12 unique digestive proteases whose expression is specific to the D. arizonae lower female reproductive tract. These enzymes belong to classes most commonly found in the gastrointestinal tracts of a diverse array of organisms. We show that these proteases are associated with recent, lineage-specific gene duplications in the Drosophila repleta species group, and exhibit strong signatures of positive selection. Observation of adaptive evolution in several female reproductive tract proteins indicates they are active players in the evolution of reproductive tract interactions. Additionally, pervasive gene duplication, adaptive evolution, and rapid acquisition of a novel digestive function by the female reproductive tract points to a novel coevolutionary mechanism of ejaculate–female interaction.

Molecular Population Genetics of Accessory Gland Protein Genes and Testis-Expressed Genes in Drosophila mojavensis and D. arizonae

Molecular population genetic investigation of Drosophila male reproductive genes has focused primarily on melanogaster subgroup accessory gland protein genes (Acp's). Consistent with observations from male reproductive genes of numerous taxa, Acp's evolve more rapidly than nonreproductive genes. However, within the Drosophila genus, large data sets from additional types of male reproductive genes and from different species groups are lacking. Here we report findings from a molecular population genetics analysis of male reproductive genes of the repleta group species, Drosophila arizonae and D. mojavensis. We find that Acp's have dramatically higher average pairwise Ka/Ks (0.93) than testis-enriched genes (0.19) and previously reported melanogaster subgroup Acp's (0.42). Overall, 10 of 19 Acp's have Ka/Ks > 1 either in nonpolarized analyses or in at least one lineage of polarized analyses. Of the nine Acp's for which outgroup data were available, average Ka/Ks was considerably higher in D. mojavensis (2.08) than in D. arizonae (0.87). Contrasts of polymorphism and divergence suggest that adaptive protein evolution at Acp's is more common in D. mojavensis than in D. arizonae.

SEXUAL SELECTION OPERATING IN A WILD POPULATION OF DROSOPHILA ROBUSTA.

Almost 60 years have elapsed since the discovery of variation in the polytene chromosomes of Drosophila (Sturtevant and Dobzhansky 1936). Inversion polymorphism studies have revealed some of the intricacies of evolutionary change, but even now, when interest in them has waned, there is little understanding of the particular alleles contained within them that alone or in relation to other genes influence any component of fitness. Perhaps the most important rule about inversion polymorphisms learned from a long history of laboratory experiments (cf. Lewontin et al. 1981) is their sensitivity to environmental features such as temperature and nutrition. Therefore, laboratory studies alone may not predict the consequences due to genotype (karyotype) by environment interactions of selection in wild populations. Only a few studies have documented selective mechanisms associated with preserving inversion polymorphisms in natural populations beyond establishing correlations with temperature, rainfall, humidity, elevation, and other environmental features. Despite the long history of interest in the ecology of Drosophila breeding and feeding sites (cf. Carson 1951, 1971; Heed 1957, 1968, 1971), experimental analyses of inversion polymorphisms involving natural breeding substrates are few because the mating sites and larval ecology of most species with well described inversion polymorphisms are poorly known, e.g., D. pseudoobscura. An early exception to this problem was the comprehensive study of inversion polymorphism in D. flavopilosa, a flower breeder from South America (Brncic 1962). Egg to adult viability differences among karyotypes were observed among preadult stages in flowers returned to the lab and exposed to contrasting temperatures (Brncic 1968). More recently, analysis of the sexratio meiotic drive system in natural populations of D. pseudoobscura suggested that most selection responsible for maintaining this polymorphism must be operating in preadult stages (Beckenbach 1996). A notable non-Drosophila example is the chromosome I polymorphism in seaweed flies, Coelopa frigida, that carry out their life cycle on decomposing seaweed on beaches around the north Atlantic and North Sea. Gene arrangement-based differences in egg to adult development time, adult body size, and mate preference have been demonstrated in seaweed-reared flies (Day et al. 1983; Engelhard et al. 1989; Gilburn et al. 1992). For species that can be collected in nature throughout their life cycle, karyotype frequencies can be estimated from life stages reared in the wild and comparisons can be made between stages of the life cycle in selection component analyses (e.g., Prout 1971; Bundgaard and Christiansen 1972). Inversion polymorphisms in cactophilic D. buzzatii have been studied this way, a species that feeds and breeds in the fermenting tissues of several species of prickly pear cactus. In general, cactophilic Drosophila have taught us much about maintenance of genetic variability, host specificity, chemical ecology, trophic adaptation, and life history evolution (Barker and Starmer 1982; Barker et al. 1990). Despite the fact that 48% (44/91) of all described and undescribed D. repleta group species possess inversion polymorphism (Wasserman 1992), in only a few species has there been concerted effort to unravel the causes for maintenance of inversion polymorphism in nature, that is, D. buzzatii and D. mojavensis. Inversion polymorphism in the latter species, along with D. pachea, a cactophilic member of the D. nannoptera group, has been recently summarized (Etges et al., in press). Ruiz et al. (1986) demonstrated endocyclic selection, directional selection in opposing directions during the life cycle, on gene arrangements of D. buzzatii. However, this pattern is population and host specific (Hasson et al. 1991) and not surprisingly is limited to a few components of fitness including egg to third instar viability and adult body size, but not mating propensity (Santos et al. 1992; Barbadilla et al. 1994). Adult size in Drosophila can be correlated with increased fitness as larger flies typically have greater reproductive potential (Robertson 1957) and dispersal ability (Mangan 1982). These studies of D. buzzatii deserve special note because they illustrate the complexity of factors that must be addressed in understanding the maintenance of inversion polymorphisms in natural populations. Thus, studies of selection on inversion polymorphisms in species with hard-to-find breeding sites have been restricted to adult flies because they can be captured in the wild. If we include the recent D. buzzatii studies mentioned above, several studies of genetic variation in male mating success (Anderson et al. 1979; Levine et al. 1980; Salceda and Anderson 1988), the recent analysis of the sex-ratio polymorphism in D. pseudoobscura (Beckenbach 1996), and mate choice in seaweed flies (Gilburn et al. 1992), most of what we know of selection operating on inversion polymorphisms under natural conditions has only recently been documented. It is interesting to note that not one example documenting an identifiable selective agent operating on inversion polymorphisms was cited by Endler (1986) in his review, Natural Selection in the Wild, despite the long history of population genetics

Molecular phylogeny and divergence times of drosophilid species.

The phylogenetic relationships and divergence times of 39 drosophilid species were studied by using the coding region of the Adh gene. Four genera--Scaptodrosophila, Zaprionus, Drosophila, and Scaptomyza (from Hawaii)--and three Drosophila subgenera--Drosophila, Engiscaptomyza, and Sophophora--were included. After conducting statistical analyses of the nucleotide sequences of the Adh, Adhr (Adh-related gene), and nuclear rRNA genes and a 905-bp segment of mitochondrial DNA, we used Scaptodrosophila as the outgroup. The phylogenetic tree obtained showed that the first major division of drosophilid species occurs between subgenus Sophophora (genus Drosophila) and the group including subgenera Drosophila and Engiscaptomyza plus the genera Zaprionus and Scaptomyza. Subgenus Sophophora is then divided into D. willistoni and the clade of D. obscura and D. melanogaster species groups. In the other major drosophilid group, Zaprionus first separates from the other species, and then D. immigrans leaves the remaining group of species. This remaining group then splits into the D. repleta group and the Hawaiian drosophilid cluster (Hawaiian Drosophila, Engiscaptomyza, and Scaptomyza). Engiscaptomyza and Scaptomyza are tightly clustered. Each of the D. repleta, D. obscura, and D. melanogaster groups is monophyletic. The splitting of subgenera Drosophila and Sophophora apparently occurred about 40 Mya, whereas the D. repleta group and the Hawaiian drosophilid cluster separated about 32 Mya. By contrast, the splitting of Engiscaptomyza and Scaptomyza occurred only about 11 Mya, suggesting that Scaptomyza experienced a rapid morphological evolution. The D. obscura and D. melanogaster groups apparently diverged about 25 Mya. Many of the D. repleta group species studied here have two functional Adh genes (Adh-1 and Adh-2), and these duplicated genes can be explained by two duplication events.

Cytology and Phylogeny of Drosophila

The rediscovery of the polytene chromosomes in the salivary glands of the Diptera has allowed for a high order of accuracy in the identification of chromosomal rearrangements. The various types of chromosomal mutations are described and their relative importance in the evolution of the genus Drosophila is briefly discussed. Paracentric inversions are the most common changes observed; and these have been used in the construction of phylogenetic trees; the repleta group where the relationships among 46 species have been determined, is used as an example of such a study. Errors in the construction of the phyletic lines resulting from observational mistakes, cytological parallelism, cytological convergence and the segregation of independent inversions are discussed. Experimental work on naturally occurring paracentric inversions indicates that the selective values of these rearrangements appear not to be correlated with their actual breakage points, but are determined by the genetic material tied together by the action of the inversion as a suppressor of recombination. The genetic content of a rearrangement varies from locality to locality: each inversion, per se, therefore, has no definable adaptive value. Survival of a newly arisen inversion is dependent upon its fortuitous occurrence in a chromosomal region which is preadapted for a recombinant suppressor, that is, the region contains cooperating loci, among which recombination would be disadvantageous. Moreover, given the conditions for preadaptation, any one of a large number of distinguishable rearrangements could equally serve the purpose. In the repleta group, only about 144 inversions have survived during the history of the 46 species studied, indicating a very low incidence of such preadaptation in this species group. In view of the above, it is felt that the occurrence and survival of a pair of indistinguishable inversions in two phyletic lines, although possible, is highly unlikely. The probability of cytological parallel or convergent evolution involving two or more indistinguishable pairs of inversions in two phyletic lines can be considered zero. Phylogenies, therefore, based on inversional changes have an exceedingly high degree of accuracy. Phylogenetic relationships among the repleta group species are shown and their evolution is briefly discussed.