Evolution of multiple additive loci caused divergence between Drosophila yakuba and D. santomea in wing rowing during male courtship

International audienceIn Drosophila, male flies perform innate, stereotyped courtship behavior. This innate behavior evolves rapidly between fly species, and is likely to have contributed to reproductive isolation and species divergence. We currently understand little about the neurobiological and genetic mechanisms that contributed to the evolution of courtship behavior. Here we describe a novel behavioral difference between the two closely related species D. yakuba and D. santomea: the frequency of wing rowing during courtship. During courtship, D. santomea males repeatedly rotate their wing blades to face forward and then back (rowing), while D. yakuba males rarely row their wings. We found little intraspecific variation in the frequency of wing rowing for both species. We exploited multiplexed shotgun genotyping (MSG) to genotype two backcross populations with a single lane of Illumina sequencing. We performed quantitative trait locus (QTL) mapping using the ancestry information estimated by MSG and found that the species difference in wing rowing mapped to four or five genetically separable regions. We found no evidence that these loci display epistasis. The identified loci all act in the same direction and can account for most of the species difference

A framework for studying behavioral evolution by reconstructing ancestral repertoires

Although extensive behavioral changes often exist between closely related animal species, our understanding of the genetic basis underlying the evolution of behavior has remained limited. Here, we propose a new framework to study behavioral evolution by computational estimation of ancestral behavioral repertoires. We measured the behaviors of individuals from six species of fruit flies using unsupervised techniques and identified suites of stereotyped movements exhibited by each species. We then fit a Generalized Linear Mixed Model to estimate the suites of behaviors exhibited by ancestral species, as well as the intra- and inter-species behavioral covariances. We found that much of intraspecific behavioral variation is explained by differences between individuals in the status of their behavioral hidden states, what might be called their "mood." Lastly, we propose a method to identify groups of behaviors that appear to have evolved together, illustrating how sets of behaviors, rather than individual behaviors, likely evolved. Our approach provides a new framework for identifying co-evolving behaviors and may provide new opportunities to study the genetic basis of behavioral evolution

A framework for studying behavioral evolution by reconstructing ancestral repertoires

Although different animal species often exhibit extensive variation in many behaviors, typically scientists examine one or a small number of behaviors in any single study. Here, we propose a new framework to simultaneously study the evolution of many behaviors. We measured the behavioral repertoire of individuals from six species of fruit flies using unsupervised techniques and identified all stereotyped movements exhibited by each species. We then fit a Generalized Linear Mixed Model to estimate the intra-and inter-species behavioral covariances, and, by using the known phylogenetic relationships among species, we estimated the (unobserved) behaviors exhibited by ancestral species. We found that much of intra-specific behavioral variation has a similar covariance structure to previously described long-time scale variation in an individual’s behavior, suggesting that much of the measured variation between individuals of a single species in our assay reflects differences in the status of neural networks, rather than genetic or developmental differences between individuals. We then propose a method to identify groups of behaviors that appear to have evolved in a correlated manner, illustrating how sets of behaviors, rather than individual behaviors, likely evolved. Our approach provides a new framework for identifying co-evolving behaviors and may provide new opportunities to study the mechanistic basis of behavioral evolution.Fil: Hernández Lahme, Damián Gabriel. University of Emory; Estados Unidos. Comisión Nacional de Energía Atómica. Gerencia del Área de Energía Nuclear. Instituto Balseiro; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte; ArgentinaFil: Rivera, Catalina. University of Emory; Estados UnidosFil: Cande, Jessica. Howard Hughes Medical Institute; Estados UnidosFil: Zhou, Baohua. University of Yale; Estados Unidos. University of Emory; Estados UnidosFil: Stern, David L.. Howard Hughes Medical Institute; Estados UnidosFil: Berman, Gordon J.. University of Emory; Estados Unido

Analysis of the Tribolium homeotic complex: insights into mechanisms constraining insect Hox clusters

The remarkable conservation of Hox clusters is an accepted but little understood principle of biology. Some organizational constraints have been identified for vertebrate Hox clusters, but most of these are thought to be recent innovations that may not apply to other organisms. Ironically, many model organisms have disrupted Hox clusters and may not be well-suited for studies of structural constraints. In contrast, the red flour beetle, Tribolium castaneum, which has a long history in Hox gene research, is thought to have a more ancestral-type Hox cluster organization. Here, we demonstrate that the Tribolium homeotic complex (HOMC) is indeed intact, with the individual Hox genes in the expected colinear arrangement and transcribed from the same strand. There is no evidence that the cluster has been invaded by non-Hox protein-coding genes, although expressed sequence tag and genome tiling data suggest that noncoding transcripts are prevalent. Finally, our analysis of several mutations affecting the Tribolium HOMC suggests that intermingling of enhancer elements with neighboring transcription units may constrain the structure of at least one region of the Tribolium cluster. This work lays a foundation for future studies of the Tribolium HOMC that may provide insights into the reasons for Hox cluster conservation

Smells like evolution: the role of chemoreceptor evolution in behavioral change.

International audienceIn contrast to physiology and morphology, our understanding of how behaviors evolve is limited. This is a challenging task, as it involves the identification of both the underlying genetic basis and the resultant physiological changes that lead to behavioral divergence. In this review, we focus on chemosensory systems, mostly in Drosophila, as they are one of the best-characterized components of the nervous system in model organisms, and evolve rapidly between species. We examine the hypothesis that changes at the level of chemosensory systems contribute to the diversification of behaviors. In particular, we review recent progress in understanding how genetic changes between species affect chemosensory systems and translate into divergent behaviors. A major evolutionary trend is the rapid diversification of the chemoreceptor repertoire among species. We focus mostly on functional comparative studies involving model species, highlighting examples where changes in chemoreceptor identity and expression are sufficient to provoke changes in neural circuit activity and thus behavior. We conclude that while we are beginning to understand the role that the peripheral nervous system (PNS) plays in behavioral evolution, how the central nervous system (CNS) evolves to produce behavioral changes is largely unknown, and we advocate the need to expand functional comparative studies to address these questions

Evolving enhancer-promoter interactions within the tinman complex of the flour beetle, Tribolium castaneum

Modifications of cis-regulatory DNAs, particularly enhancers, underlie changes in gene expression during animal evolution. Here, we present evidence for a distinct mechanism of regulatory evolution, whereby a novel pattern of gene expression arises from altered gene targeting of a conserved enhancer. The tinman gene complex (Tin-C) controls the patterning of dorsal mesodermal tissues, including the dorsal vessel or heart in Drosophila. Despite broad conservation of Tin-C gene expression patterns in the flour beetle (Tribolium castaneum), the honeybee (Apis mellifera) and the fruit fly (Drosophila melanogaster), the expression of a key pericardial determinant, ladybird, is absent from the dorsal mesoderm of Tribolium embryos. Evidence is presented that this loss in expression is replaced by expression of C15, the neighboring gene in the complex. This switch in expression from ladybird to C15 appears to arise from an inversion within the tinman complex, which redirects a conserved ladybird 3′ enhancer to regulate C15. In Drosophila, this enhancer fails to activate C15 expression owing to the activity of an insulator at the intervening ladybird early promoter. By contrast, a chromosomal inversion allows the cardiac enhancer to bypass the ladybird insulator in Tribolium. Given the high frequency of genome rearrangements in insects, it is possible that such enhancer switching might be widely used in the diversification of the arthropods

Evolution of the Ventral Midline in Insect Embryos

SummaryThe ventral midline is a source of signals that pattern the nerve cord of insect embryos. In dipterans such as the fruitfly Drosophila melanogaster (D.mel.) and the mosquito Anopheles gambiae (A.gam.), the midline is narrow and spans just 1–2 cells. However, in the honeybee, Apis mellifera (A.mel.), the ventral midline is broad and encompasses 5–6 cells. slit and other midline-patterning genes display a corresponding expansion in expression. Evidence is presented that this difference is due to divergent cis regulation of the single-minded (sim) gene, which encodes a bHLH-PAS transcription factor essential for midline differentiation. sim is regulated by a combination of Notch signaling and a Twist (Twi) activator gradient in D.mel., but it is activated solely by Twi in A.mel. We suggest that the Twi-only mode of regulation—and the broad ventral midline—represents the ancestral form of CNS patterning in Holometabolous insects

Widespread Prevalence of Wolbachia in Laboratory Stocks and the Implications for Drosophila Research

Wolbachia is an intracellular microbe harbored by a wide variety of arthropods (including Drosophila) and filarial nematodes. Employing several different strategies including male killing, induced parthenogenesis, cytoplasmic incompatibility, and feminization, and acting by as-yet-unknown mechanisms, Wolbachia alters host reproduction to increase its representation within a population. Wolbachia is closely associated with gametic incompatibility but also interacts with Drosophila in other, little understood ways. We report here significant and widespread infection of Wolbachia within laboratory stocks and its real and potential impact on Drosophila research. We describe the results of a survey indicating that ∼30% of stocks currently housed at the Bloomington Drosophila Stock Center are infected with Wolbachia. Cells of both reproductive tissues and numerous somatic organs harbor Wolbachia and display considerable variation in infection levels within and between both tissue types. These results are discussed from the perspective of Wolbachia's potential confounding effects on both host fitness and phenotypic analyses. In addition to this cautionary message, the infection status of stock centers may provide further opportunities to study the genetic basis of host/symbiosis

Stalled Hox promoters as chromosomal boundaries

Many developmental control genes contain stalled RNA Polymerase II (Pol II) in the early Drosophila embryo, including four of the eight Hox genes. Here, we present evidence that the stalled Hox promoters possess an intrinsic insulator activity. The enhancer-blocking activities of these promoters are dependent on general transcription factors that inhibit Pol II elongation, including components of the DSIF and NELF complexes. The activities of conventional insulators are also impaired in embryos containing reduced levels of DSIF and NELF. Thus, promoter-proximal stalling factors might help promote insulator–promoter interactions. We propose that stalled promoters help organize gene complexes within chromosomal loop domains

Looking under the lamp post: neither fruitless nor doublesex has evolved to generate divergent male courtship in Drosophila

International audienceHow do evolved genetic changes alter the nervous system to produce different patterns of behavior? We address this question using Drosophila male courtship behavior, which is innate, stereotyped, and evolves rapidly between species. D. melanogaster male courtship requires the male-specific isoforms of two transcription factors, fruitless and doublesex. These genes underlie genetic switches between female and male behaviors, making them excellent candidate genes for courtship behavior evolution. We tested their role in courtship evolution by transferring the entire locus for each gene from divergent species to D. melanogaster. We found that despite differences in Fru+ and Dsx+ cell numbers in wild-type species, cross-species transgenes rescued D. melanogaster courtship behavior and no species-specific behaviors were conferred. Therefore, fru and dsx are not a significant source of evolutionary variation in courtship behavior