@article {47238, title = {A major locus controls a genital shape difference involved in reproductive isolation between Drosophila yakuba and Drosophila santomea.}, journal = {G3 (Bethesda, Md.)}, volume = {5}, year = {2015}, month = {2015 Oct 28}, pages = {2893-901}, abstract = {

Rapid evolution of genitalia shape, a widespread phenomenon in animals with internal fertilization, offers the opportunity to dissect the genetic architecture of morphological evolution linked to sexual selection and speciation. Most quantitative trait loci (QTL) mapping studies of genitalia divergence have focused on Drosophila melanogaster and its three most closely related species, D. simulans, D. mauritiana, and D. sechellia, and have suggested that the genetic basis of genitalia evolution involves many loci. We report the first genetic study of male genitalia evolution between D. yakuba and D. santomea, two species of the D. melanogaster species subgroup. We focus on male ventral branches, which harm females during interspecific copulation. Using landmark-based geometric morphometrics, we characterized shape variation in parental species, F1 hybrids, and backcross progeny and show that the main axis of shape variation within the backcross population matches the interspecific variation between parental species. For genotyping, we developed a new molecular method to perform multiplexed shotgun genotyping (MSG), which allowed us to prepare genomic DNA libraries from 365 backcross individuals in a few days using little DNA. We detected only three QTL, one of which spans 2.7 Mb and exhibits a highly significant effect on shape variation that can be linked to the harmfulness of the ventral branches. We conclude that the genetic architecture of genitalia morphology divergence may not always be as complex as suggested by previous studies.

}, issn = {2160-1836}, doi = {10.1534/g3.115.023481}, author = {Peluffo, Alexandre E and Nuez, Isabelle and Debat, Vincent and Savisaar, Rosina and Stern, David L and Orgogozo, Virginie} } @article {3566, title = {Is genetic evolution predictable?}, journal = {Science}, volume = {323}, year = {2009}, month = {2009 Feb 6}, pages = {746-51}, abstract = {

Ever since the integration of Mendelian genetics into evolutionary biology in the early 20th century, evolutionary geneticists have for the most part treated genes and mutations as generic entities. However, recent observations indicate that all genes are not equal in the eyes of evolution. Evolutionarily relevant mutations tend to accumulate in hotspot genes and at specific positions within genes. Genetic evolution is constrained by gene function, the structure of genetic networks, and population biology. The genetic basis of evolution may be predictable to some extent, and further understanding of this predictability requires incorporation of the specific functions and characteristics of genes into evolutionary theory.

}, keywords = {Animals, Arabidopsis, Biological Evolution, Drosophila, Epistasis, Evolution, Gene Regulatory Networks, Genes, Genetic, Genetic Speciation, Genetic Variation, Molecular, Mutation, Phenotype, Plants, Population Dynamics, Selection}, issn = {1095-9203}, doi = {10.1126/science.1158997}, author = {Stern, David L and Orgogozo, Virginie} } @article {4409, title = {How different are recently diverged species?: more than 150 phenotypic differences have been reported for the D. melanogaster species subgroup.}, journal = {Fly}, volume = {3}, year = {2009}, month = {2009 Apr-Jun}, pages = {117}, keywords = {Animals, Drosophila melanogaster, Genetic Speciation, Phenotype, Species Specificity}, issn = {1933-6942}, author = {Orgogozo, Virginie and Stern, David L} } @article {4648, title = {The loci of evolution: how predictable is genetic evolution?}, journal = {Evolution}, volume = {62}, year = {2008}, month = {2008 Sep}, pages = {2155-77}, abstract = {

Is genetic evolution predictable? Evolutionary developmental biologists have argued that, at least for morphological traits, the answer is a resounding yes. Most mutations causing morphological variation are expected to reside in the cis-regulatory, rather than the coding, regions of developmental genes. This "cis-regulatory hypothesis" has recently come under attack. In this review, we first describe and critique the arguments that have been proposed in support of the cis-regulatory hypothesis. We then test the empirical support for the cis-regulatory hypothesis with a comprehensive survey of mutations responsible for phenotypic evolution in multicellular organisms. Cis-regulatory mutations currently represent approximately 22\% of 331 identified genetic changes although the number of cis-regulatory changes published annually is rapidly increasing. Above the species level, cis-regulatory mutations altering morphology are more common than coding changes. Also, above the species level cis-regulatory mutations predominate for genes not involved in terminal differentiation. These patterns imply that the simple question "Do coding or cis-regulatory mutations cause more phenotypic evolution?" hides more interesting phenomena. Evolution in different kinds of populations and over different durations may result in selection of different kinds of mutations. Predicting the genetic basis of evolution requires a comprehensive synthesis of molecular developmental biology and population genetics.

}, keywords = {Animals, Evolution, Humans, Molecular, Phenotype, Regulatory Elements, Transcriptional}, issn = {0014-3820}, doi = {10.1111/j.1558-5646.2008.00450.x}, author = {Stern, David L and Orgogozo, Virginie} } @article {4649, title = {Morphological evolution through multiple cis-regulatory mutations at a single gene.}, journal = {Nature}, volume = {448}, year = {2007}, month = {2007 Aug 2}, pages = {587-90}, abstract = {

One central, and yet unsolved, question in evolutionary biology is the relationship between the genetic variants segregating within species and the causes of morphological differences between species. The classic neo-darwinian view postulates that species differences result from the accumulation of small-effect changes at multiple loci. However, many examples support the possible role of larger abrupt changes in the expression of developmental genes in morphological evolution. Although this evidence might be considered a challenge to a neo-darwinian micromutationist view of evolution, there are currently few examples of the actual genes causing morphological differences between species. Here we examine the genetic basis of a trichome pattern difference between Drosophila species, previously shown to result from the evolution of a single gene, shavenbaby (svb), probably through cis-regulatory changes. We first identified three distinct svb enhancers from D. melanogaster driving reporter gene expression in partly overlapping patterns that together recapitulate endogenous svb expression. All three homologous enhancers from D. sechellia drive expression in modified patterns, in a direction consistent with the evolved svb expression pattern. To test the influence of these enhancers on the actual phenotypic difference, we conducted interspecific genetic mapping at a resolution sufficient to recover multiple intragenic recombinants. This functional analysis revealed that independent genetic regions upstream of svb that overlap the three identified enhancers are collectively required to generate the D. sechellia trichome pattern. Our results demonstrate that the accumulation of multiple small-effect changes at a single locus underlies the evolution of a morphological difference between species. These data support the view that alleles of large effect that distinguish species may sometimes reflect the accumulation of multiple mutations of small effect at select genes.

}, keywords = {Alleles, Animals, Biological, Biological Evolution, Developmental, DNA-Binding Proteins, Drosophila, Drosophila Proteins, Enhancer Elements, Evolution, Gene Expression Regulation, Genes, Genetic, Genetic Speciation, Models, Molecular, Mutation, Recombination, Reporter, Transcription Factors}, issn = {1476-4687}, doi = {10.1038/nature05988}, author = {McGregor, Alistair P and Orgogozo, Virginie and Delon, Isabelle and Zanet, Jennifer and Srinivasan, Dayalan G and Payre, Fran\c cois and Stern, David L} } @article {45742, title = {Variation in fiber number of a male-specific muscle between Drosophila species: a genetic and developmental analysis.}, journal = {Evol Dev}, volume = {9}, year = {2007}, month = {2007 Jul-Aug}, pages = {368-77}, abstract = {

We characterize a newly discovered morphological difference between species of the Drosophila melanogaster subgroup. The muscle of Lawrence (MOL) contains about four to five fibers in D. melanogaster and Drosophila simulans and six to seven fibers in Drosophila mauritiana and Drosophila sechellia. The same number of nuclei per fiber is present in these species but their total number of MOL nuclei differs. This suggests that the number of muscle precursor cells has changed during evolution. Our comparison of MOL development indicates that the species difference appears during metamorphosis. We mapped the quantitative trait loci responsible for the change in muscle fiber number between D. sechellia and D. simulans to two genomic regions on chromosome 2. Our data eliminate the possibility of evolving mutations in the fruitless gene and suggest that a change in the twist might be partly responsible for this evolutionary change.

}, keywords = {Animals, Drosophila, Genetic Variation, Male, Muscle Fibers, Skeletal, Quantitative Trait Loci}, issn = {1520-541X}, doi = {10.1111/j.1525-142X.2007.00174.x}, author = {Orgogozo, Virginie and Muro, Noelle M and Stern, David L} } @article {45749, title = {High-resolution quantitative trait locus mapping reveals sign epistasis controlling ovariole number between two Drosophila species.}, journal = {Genetics}, volume = {173}, year = {2006}, month = {2006 May}, pages = {197-205}, abstract = {

Identifying the genes underlying genetically complex traits is of fundamental importance for medicine, agriculture, and evolutionary biology. However, the level of resolution offered by traditional quantitative trait locus (QTL) mapping is usually coarse. We analyze here a trait closely related to fitness, ovariole number. Our initial interspecific mapping between Drosophila sechellia (8 ovarioles/ovary) and D. simulans (15 ovarioles/ovary) identified a major QTL on chromosome 3 and a minor QTL on chromosome 2. To refine the position of the major QTL, we selected 1038 additional recombinants in the region of interest using flanking morphological markers (selective phenotyping). This effort generated approximately one recombination event per gene and increased the mapping resolution by approximately seven times. Our study thus shows that using visible markers to select for recombinants can efficiently increase the resolution of QTL mapping. We resolved the major QTL into two epistatic QTL, QTL3a and QTL3b. QTL3a shows sign epistasis: it has opposite effects in two different genetic backgrounds, the presence vs. the absence of the QTL3b D. sechellia allele. This property of QTL3a allows us to reconstruct the probable order of fixation of the QTL alleles during evolution.

}, keywords = {Animals, Chromosome Mapping, Chromosomes, Crosses, Genetic, Drosophila, Epistasis, Genetic, Evolution, Molecular, Female, Ovary, Quantitative Trait Loci}, issn = {0016-6731}, doi = {10.1534/genetics.105.054098}, author = {Orgogozo, Virginie and Broman, Karl W and Stern, David L} }