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David, J. R.

Publications and source records attributed to David, J. R..

9 recordsLinked to original sources

Phenotypic plasticity as a function of genetic polymorphism: thermal dominance reversal in Drosophila species with contrasting melanism

Phenotypic plasticity is often seen as an alternative adaptive strategy to genetic polymorphism, especially in response to rapid environmental changes. Indeed, a link between plasticity and heterozygosity, i.e. the measure of polymorphism, has previously been dismissed. Here, we compare the thermal plasticity of abdominal pigmentation in eight Drosophila species, four belonging to the melanogaster species group and four to the montium group. Despite a conserved developmental pathway for melanin synthesis, the genetic architecture of its variation has significantly evolved, being polygenic in most species (like D. melanogaster) and Mendelian or invariable in others. By investigating the thermal plasticity of this trait in species with distinct architectures, we show the degree of plasticity to strongly associate with heterozygosity. Plasticity was resurrected in hybrids between species with no plastic responses but with contrasting melanism, and was higher in heterozygotes in species with simple Mendelian polymorphism. In plastic cases, pigmentation dominance is reversed depending on the developmental temperature. We propose simple genetic models with empirical molecular support to explain this link between phenotypic plasticity and genetic polymorphism. The relationship between these two phenomena, and the impact of each on the evolution of the other, may be more relevant than it is currently appreciated.

evolutionary biology↗

Evolution of assortative mating following selective introgression of pigmentation genes between two Drosophila species

Adaptive introgression is ubiquitous in animals but experimental support for its role in driving speciation remains scarce. In the absence of conscious selection, admixed laboratory strains of Drosophila asymmetrically and progressively lose alleles from one parental species and reproductive isolation against the predominant parent ceases after 10 generations. Here, we selectively introgressed during one year light pigmentation genes of D. santomea into the genome of its dark sibling D. yakuba, and vice versa. We found that the pace of phenotypic change differed between the species and the sexes, and identified through genome sequencing common as well as distinct introgressed loci in each species. Mating assays showed that assortative mating between introgressed flies and both parental species persisted even after four years ([~] 60 generations) from the end of the selection. Those results indicate that selective introgression of as low as 0.5% of the genome can beget morphologically-distinct and reproductively-isolated strains, two prerequisites for the delimitation of new species. Our findings hence represent a significant step towards understanding the genome-wide dynamics of speciation-through-introgression.

evolutionary biology↗

Long-term evolution of quantitative traits in the Drosophila melanogaster species subgroup

Quantitative genetics aims at untangling the genetic and environmental effects on phenotypic variation. Trait heritability, which summarizes the relative importance of genetic effects, is estimated at the intraspecific level, but theory predicts that heritability could influence long-term evolution of quantitative traits. The phylogenetic signal concept bears resemblance to heritability and it has often been called species-level heritability. Under certain conditions, such as trait neutrality or contribution to phylogenesis, within-species heritability and between-species phylogenetic signal should be correlated. Here, we investigate the potential relationship between these two concepts by examining the evolution of multiple morphological traits for which heritability has been estimated in Drosophila melanogaster. Specifically, we analysed 42 morphological traits in both sexes on a phylogeny inferred from 22 nuclear genes for nine species of the melanogaster subgroup. We used Pagels {lambda} as a measurement of phylogenetic signal because it is the least influenced by the number of analysed taxa. Pigmentation traits showed the strongest concordance with the phylogeny, but no correlation was found between phylogenetic signal and heritability estimates mined from the literature. We obtained data for multiple climatic variables inferred from the geographical distribution of each species. Phylogenetic regression of quantitative traits on climatic variables showed a significantly positive correlation with heritability. Convergent selection, the response to which depends on the trait heritability, may have led to the null association between phylogenetic signal and heritability for morphological traits in Drosophila. We discuss the possible causes of discrepancy between both statistics and caution against their confusion in evolutionary biology.

evolutionary biology↗

Divergent phenotypic plasticity of a convergent Mendelian trait in Drosophila

In Drosophila, comparisons of the thermal plasticity of pigmentation across serially homologous abdominal segments have been conducted in two species, namely Drosophila melanogaster and D. kikkawai. Pigmentation variation has different genetic architecture in the two species, being oligogenic in the former and monogenic in the later. Here, we analyze the thermal plasticity of abdominal pigmentation in a third species, D. erecta, which is phylogenetically close to D. melanogaster but like D. kikkawai has a monogenic basis for pigmentation variation. However, the underlying locus differs between D. erecta and D. kikkawai, being the X-linked melanin-synthesis gene tan in the former and the autosomal transcription factor pdm3 in the later. We found that in spite of a low overall plasticity in monogenic species compared to D. melanogaster, the two monogenic species showed divergent plasticity patterns in respect to the response to temperature and to the degree of dominance in heterozygotes. Those results provide new insights on the dependence of the degree of plasticity on the genetic architecture as well as on the extent of phenotypic convergence.

evolutionary biology↗

Resolving Between Novelty and Homology in the Rapidly Evolving Phallus of Drosophila

The genitalia present some of the most rapidly evolving anatomical structures in the animal kingdom, possessing a variety of parts that can distinguish recently diverged species. In the Drosophila melanogaster group, the phallus is adorned with several processes, pointed outgrowths, that are similar in size and shape between species. However, the complex three-dimensional nature of the phallus can obscure the exact connection points of each process. Previous descriptions based upon adult morphology have primarily assigned phallic processes by their approximate positions in the phallus and have remained largely agnostic regarding their homology relationships. In the absence of clearly identified homology, it can be challenging to model when each structure first evolved. Here, we employ a comparative developmental analysis of these processes in eight members of the melanogaster species group to precisely identify the tissue from which each process forms. Our results indicate that adult phallic processes arise from three pupal primordia in all species. We found that in some cases the same primordia generate homologous structures whereas in other cases, different primordia produce phenotypically similar but remarkably non-homologous structures. This suggests that the same gene regulatory network may have been redeployed to different primordia to induce phenotypically similar traits. Our results highlight how traits diversify and can be redeployed, even at short evolutionary scales. Research HighlightBy incorporating developmental analysis, we find that genital structures previously identified as homologs are novel structures. This highlights how developmental analysis can help resolve contentious claims of homology.

evolutionary biology↗

Widespread introgression across a phylogeny of 155 Drosophila genomes

Genome-scale sequence data have invigorated the study of hybridization and introgression, particularly in animals. However, outside of a few notable cases, we lack systematic tests for introgression at a larger phylogenetic scale across entire clades. Here we leverage 155 genome assemblies, from 149 species, to generate a fossil-calibrated phylogeny and conduct multilocus tests for introgression across nine monophyletic radiations within the genus Drosophila. Using complementary phylogenomic approaches, we identify widespread introgression across the evolutionary history of Drosophila. Mapping gene-tree discordance onto the phylogeny revealed that both ancient and recent introgression has occurred across most of the nine clades that we examined. Our results provide the first evidence of introgression occurring across the evolutionary history of Drosophila and highlight the need to continue to study the evolutionary consequences of hybridization and introgression in this genus and across the Tree of Life.

evolutionary biology↗

Temperature change has the same effect as genetic variation on a morphological trait involved in reproductive isolation between Drosophila sister species

Male genitalia are usually extremely divergent between closely related species, but relatively constant within one species. Here we examine the effect of temperature on the shape of the ventral branches, a male genital structure involved in reproductive isolation, in the sister species Drosophila santomea and D. yakuba. We designed a semi-automatic measurement pipeline that can reliably identify curvatures and landmarks based on manually digitized contours of the ventral branches. With this method, we observed that temperature does not affect ventral branches in D. yakuba but that in D. santomea ventral branches tend to morph into a D. yakuba-like shape at lower temperature. Our results suggest that speciation of D. santomea and D. yakuba was associated with a change in genitalia plasticity.

evolutionary biology↗

Correlated Evolution of two Sensory Organs via a Single Cis-Regulatory Nucleotide Change

Diverse traits often covary between species. The possibility that a single mutation could contribute to the evolution of several characters between species is rarely investigated as relatively few cases are dissected at the nucleotide level. Drosophila santomea has evolved additional sex comb sensory teeth on its legs and has lost two sensory bristles on its genitalia. We found that a single nucleotide substitution in an enhancer of the scute gene contributes to both changes. The mutation alters a binding site for the Hox protein Abdominal-B in the developing genitalia, leading to bristle loss, and for another factor in the developing leg, leading to bristle gain. Our study shows that morphological evolution between species can occur through a single nucleotide change affecting several sexually dimorphic traits.\n\nOne Sentence SummaryWe identify one nucleotide substitution in a gene regulatory region contributing to evolutionary change of two distinct organs.

evolutionary biology↗

The Rate Of Evolution Of Postmating-Prezygotic Reproductive Isolation In Drosophila

Reproductive isolation (RI) is an intrinsic aspect of species, as described in the Biological Species Concept. For that reason, the identification of the precise traits and mechanisms of RI, and the rates at which they evolve, is crucial to understanding how species originate and persist. Nonetheless, precise measurements of the magnitude of reproductive isolation are rare. Previous work has measured the rates of evolution of prezygotic and postzygotic barriers to gene flow, yet no systematic analysis has carried out the study of the rates of evolution of postmating-prezygotic (PMPZ) barriers. We systematically measured the magnitude of two barriers to gene flow that act after mating occurs but before zygotic fertilization and also measured a premating (female mating rate in nonchoice experiments) and two postzygotic barriers (hybrid inviability and hybrid sterility) for all pairwise crosses of species within the Drosophila melanogaster subgroup. Our results indicate that PMPZ isolation evolves faster than hybrid inviability but slower than premating isolation. We also describe seven new interspecific hybrids in the group. Our findings open up a large repertoire of tools that will enable researchers to manipulate hybrids and explore the genetic basis of interspecific differentiation, reproductive isolation, and speciation.

evolutionary biology↗