Isolation In Drosophila Research Articles

The evolution of seminal fluid gene expression and postmating reproductive isolation in Drosophila.

Seminal fluid protein (Sfp) genes show, in general, a higher rate of sequence divergence than genes from other categories, which is often attributed to forms of postcopulatory sexual selection or sexual conflict. Recently, the relaxation of selective constraints has been proposed as an alternative explanation for the rapid sequence evolution of Sfps and other genes with sex-limited expression. The expression of Sfp genes is a likely target of selection, but the evolution of differences in their expression levels is less understood. Here, we explore both polymorphism and divergence in Sfp gene expression between Drosophila melanogaster and Drosophila simulans, how selection might have influenced their expression, and whether changes in expression might trigger the evolution of reproductive isolating barriers. In our analysis, Sfp genes showed higher divergence, but not higher polymorphism, in expression than the average male reproductive glands gene. Sfp genes with reproductive-tissue-specific expression were enriched for both directional and stabilizing selection, while relaxed selection was the predominant mode of evolution among Sfp genes with any other nonreproductive tissue-specific or nontissue-specific expression. The knockdown of single genes known to affect intraspecific sperm competition, and with patterns of expression divergence and polymorphism suggestive of directional selection, was not enough to break down postmating reproductive isolation barriers between species. Our results identify the expression of male-specific Sfp genes as an enriched target of selection and suggest a complex molecular relationship between postcopulatory sexual selection on a single gene's expression and its effect on the onset of speciation.

The Integrity of the HMR complex is necessary for centromeric binding and reproductive isolation in Drosophila.

Postzygotic isolation by genomic conflict is a major cause for the formation of species. Despite its importance, the molecular mechanisms that result in the lethality of interspecies hybrids are still largely unclear. The genus Drosophila, which contains over 1600 different species, is one of the best characterized model systems to study these questions. We showed in the past that the expression levels of the two hybrid incompatibility factors Hmr and Lhr diverged in the two closely related Drosophila species, D. melanogaster and D. simulans, resulting in an increased level of both proteins in interspecies hybrids. The overexpression of the two proteins also leads to mitotic defects, a misregulation in the expression of transposable elements and decreased fertility in pure species. In this work, we describe a distinct six subunit protein complex containing HMR and LHR and analyse the effect of Hmr mutations on complex integrity and function. Our experiments suggest that HMR needs to bring together components of centromeric and pericentromeric chromatin to fulfil its physiological function and to cause hybrid male lethality.

Incompatibility Between X Chromosome Factor and Pericentric Heterochromatic Region Causes Lethality in Hybrids Between Drosophila melanogaster and Its Sibling Species

The Dobzhansky-Muller model posits that postzygotic reproductive isolation results from the evolution of incompatible epistatic interactions between species: alleles that function in the genetic background of one species can cause sterility or lethality in the genetic background of another species. Progress in identifying and characterizing factors involved in postzygotic isolation in Drosophila has remained slow, mainly because Drosophila melanogaster, with all of its genetic tools, forms dead or sterile hybrids when crossed to its sister species, D. simulans, D. sechellia, and D. mauritiana. To circumvent this problem, we used chromosome deletions and duplications from D. melanogaster to map two hybrid incompatibility loci in F(1) hybrids with its sister species. We mapped a recessive factor to the pericentromeric heterochromatin of the X chromosome in D. simulans and D. mauritiana, which we call heterochromatin hybrid lethal (hhl), which causes lethality in F(1) hybrid females with D. melanogaster. As F(1) hybrid males hemizygous for a D. mauritiana (or D. simulans) X chromosome are viable, the lethality of deficiency hybrid females implies that a dominant incompatible partner locus exists on the D. melanogaster X. Using small segments of the D. melanogaster X chromosome duplicated onto the Y chromosome, we mapped a dominant factor that causes hybrid lethality to a small 24-gene region of the D. melanogaster X. We provide evidence suggesting that it interacts with hhl(mau). The location of hhl is consistent with the emerging theme that hybrid incompatibilities in Drosophila involve heterochromatic regions and factors that interact with the heterochromatin.

Preliminary report on artificial selection towards sexual isolation in Drosophila.

Preliminary report on artificial selection towards sexual isolation in Drosophila.

ADAPTATION TO DESICCATION FAILS TO GENERATE PRE- AND POSTMATING ISOLATION IN REPLICATEDROSOPHILA MELANOGASTERLABORATORY POPULATIONS

Many laboratory speciation experiments have raised allopatric populations in different environments to determine whether reproductive isolation evolves as a byproduct of adaptation (a form of ecological speciation). Few, however, have addressed the evolution of both pre- and postmating isolation or investigated the conditions affecting the process. We present results of an evolution experiment in which 12 lines of Drosophila melanogaster were derived from a common population and then independently evolved for more than 57 generations under alternative selection treatments. Six "desiccation" populations had access to food and water removed during a period of their adult lives generating strong desiccation selection, and six "starvation" populations had access to food but not water removed for the same period, generating a mild starvation stress. Substantial divergence of cuticular hydrocarbons occurred between the desiccation and starvation populations, key traits that have been implicated in sexual isolation in Drosophila. Despite this divergence, there was no detectable premating isolation between desiccation and starvation populations and postmating isolation was asymmetrical: the fitness of F1 hybrids was reduced in the desiccation but not the starvation environment. This asymmetry was likely caused by the absence of divergent selection: adaptation to desiccation appears to have come at no cost to performance in the starvation environment. Novel environments are thought to promote the evolution of reproductive isolation. Understanding the conditions that favor or hamper this remains a key challenge for speciation research.

SPECIES HYBRIDS IN THE LABORATORY BUT NOT IN NATURE: A REANALYSIS OF PREMATING ISOLATION BETWEENDROSOPHILA ARIZONAEANDD. MOJAVENSIS

Understanding speciation relies critically on the identification of mechanisms responsible for maintaining species integrity (i.e., reproductive isolation) especially when closely related species are sympatric in nature. Studies of reproductive isolation in Drosophila often involve laboratory mating experiments that assume that patterns of mate choice in the laboratory are similar to those in the wild. Two sibling species, Drosophila arizonae and D. mojavensis, known to exhibit low levels of interspecific hybridization in the laboratory, but not in nature, were used in multiple-choice mating trials using various mating chamber designs as well as synthetic and natural media for developing larvae and courting adults. Sympatric populations were more sexually isolated than allopatric ones, consistent with past studies, and all experimental variables tested (chamber size, host plant presence and rearing substrates) had significant effects on levels of premating isolation between these species. Flies reared on cactus showed increased premating isolation versus those reared on synthetic laboratory food as did providing fermenting host plant tissue during mating trials. Also, surprisingly, smaller mating chambers led to an increase in premating isolation versus larger containers. The design of these types of mating trials is thus critical to understanding how mating behaviors in the laboratory are related to those in natural populations.

Effects of Social Isolation on Neuromuscular Excitability and Aggressive Behaviors in Drosophila: Altered Responses by Hk and gsts1, Two Mutations Implicated in Redox Regulation

Social deprivation is known to trigger a variety of behavioral and physiological modifications in animal species, but the underlying genetic and cellular mechanisms are not fully understood. As we described previously, adult female flies reared in isolation show increased frequency of aggressive behaviors than those reared in a group. Here, we report that isolated rearing also caused significantly altered nerve and muscle excitability and enhanced synaptic transmission at larval neuromuscular junctions (NMJs). We found that mutations of two genes, Hyperkinetic (Hk) and glutathione S-transferase-S1 (gsts1), alter the response to social isolation in Drosophila. Hk and gsts1 mutations increased adult female aggression and larval neuromuscular hyperexcitability, even when reared in a group. Unlike wild type, these behavioral and electrophysiological phenotypes were not further enhanced in these mutants by isolated rearing. Products of these two genes have been implicated in reactive oxygen species (ROS) metabolism. We previously reported in these mutants increased signals from an ROS probe at larval NMJs, and this study revealed distinct effects of isolation rearing on these mutants, compared to the control larvae in ROS-probe signals. Our data further demonstrated modified nerve and muscle excitability by a reducing agent, dithiothreitol. Our results suggest that altered cellular ROS regulation can exert pleiotropic effects on nerve, synapse, and muscle functions and may involve different redox mechanisms in different cell types to modify behavioral expressions. Therefore, ROS regulation may take part in the cellular responses to social isolation stress, underlying an important form of neural and behavioral plasticity.

Viviparity‐driven Conflict

Equipped with Mendel's laws and only rudimentary knowledge of genes and genomes, the architects of the Modern Synthesis provided key insights into the dynamics of gene frequency change within populations. Extension of population genetic models to speciation identified Dobzhansky-Muller incompatibilities (negative epistatic interactions between genes from isolated populations) as the primary cause of hybrid inviability and sterility, a view consistent with empirical findings on the genetics of reproductive isolation in Drosophila. Although speciation models have become increasingly mathematically sophisticated, many remain based on an overly static concept of the genome, grounded in Mendelian genetics and devoid of potentially important biological details. A unifying theory of speciation therefore remains elusive, with debate over the relative importance of natural selection, sexual selection, sexual conflict, genetic drift, and selfish genetic elements in the evolution of reproductive isolation. Drawing on recent findings in molecular genetics and comparative genomics, we revisit, update, and extend the theory that reproductive mode plays a crucial role in shaping the speciation process. By providing a direct conduit for manipulation of the mother's physiology by genes expressed in the embryo, viviparity creates a postfertilization arena for genomic conflicts absent in species that lay eggs. In polyandrous species, viviparity-driven conflict (VDC) is likely to generate perpetual antagonistic coevolution between genes expressed during embryonic development and those involved in maternal reproductive physiology, thereby accelerating the rate at which postzygotic isolation evolves between populations. Moreover, in mammals and flowering plants, VDC has favored the evolution of genomic imprinting and a central role for epigenetic mechanisms in the regulation of antagonistic patterns of gene expression by maternally and paternally inherited genomes. VDC can account for the rapid rate at which mammals and viviparous fishes lose their ability to hybridize; the key role of the triploid endosperm in postzygotic reproductive isolation in flowering plants; and the kinds of traits, genes, and gene regulatory systems most critical to the evolution of postzygotic reproductive isolation in live-bearing species.

Nocturnal Male Sex Drive in Drosophila

Many behaviors and physiological processes including locomotor activity, feeding, sleep, mating, and migration are dependent on daily or seasonally reoccurring, external stimuli. In D. melanogaster, one of the best-studied circadian behaviors is locomotion. The fruit fly is considered a diurnal (day active/night inactive) insect, based on locomotor-activity recordings of single, socially naive flies. We developed a new circadian paradigm that can simultaneously monitor two flies in simple social contexts. We find that heterosexual couples exhibit a drastically different locomotor-activity pattern than individual males, females, or homosexual couples. Specifically, male-female couples exhibit a brief rest phase around dusk but are highly active throughout the night and early morning. This distinct locomotor-activity rhythm is dependent on the clock genes and synchronized with close-proximity encounters, which reflect courtship, between the male and female. The close-proximity rhythm is dependent on the male and not the female and requires circadian oscillators in the brain and the antenna. Taken together, our data show that constant exposure to stimuli emanating from the female and received by the male olfactory and other sensory systems is responsible for the significant shift in intrinsic locomotor output of socially interacting flies.

Reproductive Tract Interactions Contribute to Isolation in Drosophila

Understanding how new species arise remains a persistent challenge in evolutionary biology. Extensive studies on a range of organisms have shown that the speciation process is complex and involves the development of several mechanisms for reproductive isolation. Recently, it has been hypothesized that postcopulatory-prezygotic isolation, which occurs in the female reproductive tract, may play an important role in speciation. Empirical evidence of specific incompatibilities, however, remains sparse. Here we use matings between two related species of Drosophila, D. mojavensis and D. arizonae, to demonstrate the role of reproductive tract interactions in speciation and to identify aberrant phenotypes in heterospecifically mated females.

X chromosomes and autosomes evolve at similar rates in Drosophila: no evidence for faster-X protein evolution.

Recent data from Drosophila suggest that a substantial fraction of amino acid substitutions observed between species are beneficial. If these beneficial mutations are on average partially recessive, then the rate of protein evolution is predicted to be faster for X-linked genes compared to autosomal genes (the "faster-X" hypothesis). We test this prediction by comparing rates of protein substitutions between orthologous genes, taking advantage of variations in chromosome fusions within the genus Drosophila. In members of the Drosophila melanogaster species group, the chromosomal arm 3L segregates as an ordinary autosome (i.e., two homologous copies in both males and females). However, in the Drosophila pseudoobscura species group, this chromosomal arm has become fused to the ancestral X chromosome and is hemizygous in males. The faster-X hypothesis predicts that protein evolution should be faster for genes on this chromosomal arm in the D. pseudoobscura lineage, relative to the D. melanogaster lineage. Here we combine new sequence data for 202 gene fragments in Drosophila miranda (in the pseudoobscura species group) with the completed genomes of D. melanogaster, D. pseudoobscura, and Drosophila yakuba to show that there are no detectable differences in rates of amino acid evolution for orthologous X-linked and autosomal genes. Our results imply that the contribution of the faster-X (if any) to the large-X effect on reproductive isolation in Drosophila is not due to a generally faster rate of protein evolution. The lack of a detectable faster-X effect in these species suggests either that beneficial amino acids are not partially recessive on average, or that adaptive evolution does not often use newly arising amino acid mutations.

Is premating isolation in Drosophila overestimated due to uncontrolled factors?

Sexual isolation in Drosophila is typically measured by multiple-choice mating tests. While many environmental variables during such tests are controlled by the researcher, there are some factors that are usually uncontrolled. We demonstrate, using Drosophila melanogaster and D. pseudoobscura flies, that the temperature of rearing, pre-adult density, and level of consanguinity, can all produce differences in mating propensity between genetically equivalent flies. These differences in mating propensity, in turn, can give rise to statistically significant results in multiple-choice mating tests, leading to positive isolation values and the artifactual inference of sexual isolation between populations. This fact agrees with a nonrandom excess of significant positive tests found in a review of the literature of Drosophila intraspecific mating choice. An overestimate of true cases of sexual isolation in Drosophila in the literature can, therefore, not be ruled out.

Hybrids between Chorthippus brunneus and C. jacobsi (Orthoptera: Acrididae) do not show endogenous postzygotic isolation

Studies of prezygotic and postzygotic isolation in Drosophila have shown in general that species in sympatry tend to evolve prezygotic barriers earlier than do species in allopatry. However, postzygotic barriers tend to evolve at the same evolutionary rate in both sympatric and allopatric species. In contrast to these observations, the grasshoppers Chorthippus parallelus parallelus and C. p. erythropus show complete hybrid male sterility but only limited prezygotic isolation after an estimated 0.5 millions years of divergence. Like their congeners, C. brunneus and C. jacobsi form a hybrid zone where their ranges meet in northern Spain. However, the hybrid zone is mosaic and bimodal and, in contrast to the high levels of postzygotic isolation between C. parallelus subspecies, these two species showed no significant reduction in hybrid fitness in F1 or backcross generations relative to the parental generations. The level of prezygotic isolation in laboratory tests was comparable to that between C. parallelus subspecies. These results suggest that endogenous postzygotic isolation does not play an important role in the reproductive isolation between C. brunneus and C. jacobsi, or in determining the structure of the hybrid zone. Exogenous postzygotic isolation may be present and should be tested in future studies. © 2005 The Linnean Society of London, Biological Journal of the Linnean Society, 2005, 84, 195–203.

A rapidly evolving MYB-related protein causes species isolation in Drosophila.

Matings among different species of animals or plants often result in sterile or lethal hybrids. Identifying the evolutionary forces that create hybrid incompatibility alleles is fundamental to understanding the process of speciation, but very few such alleles have been identified, particularly in model organisms that are amenable to experimental manipulation. We report here the cloning of the first, to our knowledge, Drosophila melanogaster gene involved in hybrid incompatibilities, Hybrid male rescue (Hmr). Hmr causes lethality and female sterility in hybrids among D. melanogaster and its sibling species. We have found that Hmr encodes a protein with homology to a family of MYB-related DNA-binding transcriptional regulators. The HMR protein has evolved both amino acid substitutions and insertions and deletions at an extraordinarily high rate between D. melanogaster and its sibling species, including in its predicted DNA-binding domain. Our results suggest that hybrid lethality may result from disruptions in gene regulation, and we also propose that rapid evolution may be a hallmark of speciation genes in general.

X-linked small GTPase and OXPHOS genes are candidates for the genetic basis of hybrid inviability in Drosophila.

Genetic studies on postmating reproductive isolation in Drosophila have suggested that the genetic basis of hybrid inviability is much less complex than the basis of hybrid sterility, and may be associated with defects affecting the cell cycle. Here I report the identification of a cluster of genes in the middle of the X chromosome of D. melanogaster, which may be responsible for the inviability of hybrids between Drosophila species. Genes from this cluster code for small Ras GTPases proteins, which are hypothesized here to interact with proteins involved in oxidative phosphorylation (OXPHOS), encoded by genes present within the same cluster. At least six genes influencing small Ras GTPases/OXPHOS activity are transcribed from the same strand across 35 kb genomic DNA. This interval is predicted to harbor genes which, when mutated, rescue otherwise inviable hybrids between D. melanogaster and its three most closely related species. Moreover, a total of 16 small GTPase/OXPHOS genes are found within 530 kb genomic DNA encompassing the above cluster. In D. melanogaster mutants which fully rescue lethal hybrids, major lesions have now been identified very near or within untranslated regions of two OXPHOS genes from the above cluster. These observations led to a hypothesis focusing on antagonistic co-evolution between biparentally inherited genes influencing putative GTPase/OXPHOS activity and mitochondrial genes encoding OXPHOS proteins. Alterations in some of these genes are postulated to override hybrid inviability, thus revealing a pathway which implicates mitotic genes as critical players in this barrier to reproduction.

A locus for female discrimination behavior causing sexual isolation in Drosophila.

The genetic basis of sexual isolation that contributes to speciation is one of the unsolved questions in evolutionary biology. Drosophila ananassae and Drosophila pallidosa are closely related, and postmating isolation has not developed between them. However, females of both species discriminate their mating partners, and this discrimination contributes to strong sexual isolation between them. By using surgical treatments, we demonstrate that male courtship songs play a dominant role in female mate discrimination. The absence of the song of D. pallidosa dramatically increased interspecies mating with D. ananassae females but reduced intraspecies mating with D. pallidosa females. Furthermore, genetic analysis and chromosomal introgression by repeated backcrosses to D. pallidosa males identified possible loci that control female discrimination in each species. These loci were mapped on distinct positions near the Delta locus on the middle of the left arm of the second chromosome. Because the mate discrimination we studied is well developed and is the only known mechanism that prevents gene flow between them, these loci may have played crucial roles in the evolution of reproductive isolation, and therefore, in the speciation process between these two species.

Recombination, statistical power, and genetic studies of sexual isolation in Drosophila.

Genetic studies of sexual isolation in Drosophila have generally failed to fully evaluate the effects of their sample size and recombination between markers on their conclusions. In this study we evaluate recombinational distances between markers in Drosophila pseudoobscura and D. persimilis, a species pair in which numerous genetic mapping studies have been performed. We conclude that, contrary to assertions, the inversions that distinguish these two species still allow for much recombination within most of their chromosome arms in F1 hybrid females. Such recombination may have caused previous mapping studies in these species to miss (or grossly underestimate) the effects of several genomic regions. We also evaluate the effects of sample size and recombination on genetic studies of sexual isolation in other Drosophila species groups. We conclude that some of these studies may have been heavily biased toward detecting only genes of large effect. Future studies of sexual isolation should be preceded by detailed statistical power analyses that determine the effects of recombination and sample size in the species pair being studied to avoid these complications.

The Effects of Selection and Bottlenecks on Male Mating Success in Peripheral Isolates

Previous articleNext article No AccessNotes and CommentsThe Effects of Selection and Bottlenecks on Male Mating Success in Peripheral IsolatesArne Ø. Mooers, Howard D. Rundle, Michael C. Whitlock, and Associate Editor: Nicholas BartonArne Ø. Mooers*To whom correspondence should be addressed; e‐mail: [email protected]. Search for more articles by this author , Howard D. Rundle†E‐mail: [email protected]. Search for more articles by this author , Michael C. Whitlock‡E‐mail: [email protected]. Search for more articles by this author , and Associate Editor: Nicholas Barton Search for more articles by this author 1Department of Zoology and Centre for Biodiversity Research, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada; 2Institute for Systematics and Population Biology and Zoological Museum, University of Amsterdam, P.O. Box 94766, Amsterdam 1090GT, The NetherlandsPDFPDF PLUSFull Text Add to favoritesDownload CitationTrack CitationsPermissionsReprints Share onFacebookTwitterLinkedInRedditEmail SectionsMoreDetailsFiguresReferencesCited by The American Naturalist Volume 153, Number 4April 1999 Published for The American Society of Naturalists Article DOIhttps://doi.org/10.1086/303186 Views: 80Total views on this site Citations: 24Citations are reported from Crossref HistoryReceived July 10, 1998Accepted November 13, 1998 Keywordsperipheral isolatesinbreedingmate choicemating successgene flowspeciation genetics© 1999 by The University of Chicago.PDF download Crossref reports the following articles citing this article:Elena G. Belkina, Elena B. Naimark, Anastasiya A. Gorshkova, Alexander V. Markov Does adaptation to different diets result in assortative mating? 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Reproductive isolation in Drosophila: how close are we to untangling the genetics of speciation?

Our understanding of the genetic basis of reproductive isolation in Drosophila has progressed rapidly over the past decade. Details of the genetic structure of hybrid sterility have been revealed and a general consensus has been reached concerning the genetic bases of Haldane's rule. Genetic analyses now reach beyond hybrid sterility and inviability, allowing us to make important comparisons across different traits involved in reproductive isolation. Expansion of genetic studies to include rescue of hybrid incompatibilities has opened the door for more detailed molecular and developmental analyses of reproductive isolation than has ever before been possible.

Sexual Isolation inDrosophila. III. Estimating Isolation Using Male-choice Experiments

It has been generally assumed that “choice experiments” are useful to measure sexual isolation betweenDrosophilastrains or species. Theoretical models have demonstrated however that the results obtained using one of these designs, namely multiple-choice experiments, are insufficient to determine the degree of isolation, even under very favorable assumptions. In this work, a simple behavioral model is developed to test whether male-choice experiments can be used to measure sexual isolation inDrosophila. This model shows that, although the outcome of male-choice experiments is affected by differences in female receptivities, a procedure to estimate the minimum degree of isolation using this experimental design can be established. The application of the methods derived from the theoretical model to previously reported experimental data demonstrates that a substantial degree of isolation frequently exists intraspecifically, while isolation is far from complete interspecifically. These results have important implications for discussions based on the comparative analysis ofDrosophilabehavior, both intra- and interspecifically. Most especially, they are in contradiction with the expectations of the Recognition concept of species.