Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba

Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations

Correlated evolution of male and female reproductive traits drive a cascading effect of reinforcement in Drosophila yakuba

Selection against maladaptive hybridization can drive the evolution of reproductive isolation in a process called reinforcement. While the importance of reinforcement in evolution has been historically debated, many examples now exist. Despite these examples, we typically lack a detailed understanding of the mechanisms limiting the spread of reinforced phenotypes throughout a species' range. Here we address this issue in the fruit fly Drosophila yakuba, a species that hybridizes with its sister species D. santomea and is undergoing reinforcement in a well-defined hybrid zone on the island of São Tomé. Within this region, female D. yakuba show increased postmating-prezygotic (gametic) isolation towards D. santomea when compared with females from allopatric populations. We use a combination of natural collections, fertility assays, and experimental evolution to understand why reinforced gametic isolation in D. yakuba is confined to this hybrid zone. We show that, among other traits, D. yakuba males from sympatric populations sire fewer progeny than allopatric males when mated to allopatric D. yakuba females. Our results provide a novel example of reinforcement acting on a postmating-prezygotic trait in males, resulting in a cascade of reproductive isolation among conspecific populations

Revisiting an Old Riddle: What Determines Genetic Diversity Levels within Species?

Understanding why some species have more genetic diversity than others is central to the study of ecology and evolution, and carries potentially important implications for conservation biology. Yet not only does this question remain unresolved, it has largely fallen into disregard. With the rapid decrease in sequencing costs, we argue that it is time to revive it.</p

The genomes of two key bumblebee species with primitive eusocial organization

Background: The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some species. High-quality genomic data will inform key aspects of bumblebee biology, including susceptibility to implicated population viability threats. Results: We report the high quality draft genome sequences of Bombus terrestris and Bombus impatiens, two ecologically dominant bumblebees and widely utilized study species. Comparing these new genomes to those of the highly eusocial honeybee Apis mellifera and other Hymenoptera, we identify deeply conserved similarities, as well as novelties key to the biology of these organisms. Some honeybee genome features thought to underpin advanced eusociality are also present in bumblebees, indicating an earlier evolution in the bee lineage. Xenobiotic detoxification and immune genes are similarly depauperate in bumblebees and honeybees, and multiple categories of genes linked to social organization, including development and behavior, show high conservation. Key differences identified include a bias in bumblebee chemoreception towards gustation from olfaction, and striking differences in microRNAs, potentially responsible for gene regulation underlying social and other traits. Conclusions: These two bumblebee genomes provide a foundation for post-genomic research on these key pollinators and insect societies. Overall, gene repertoires suggest that the route to advanced eusociality in bees was mediated by many small changes in many genes and processes, and not by notable expansion or depauperation

Exploring the evolution of social behaviour using genomic data

Sociality is at the root of tremendous ecological success of several taxa, including humans, ants, bees, wasps and termites. The degree and type of sociality varies greatly across taxa. The evolution of complex social behaviour can be studied by performing comparative analyses of organisms across a phylogeny showing diverse social lifestyles. We chose bees as model systems for this study because a wide range of social behaviour patterns, ranging from highly eusocial to solitary can be found in extant bees. Our aim is to identify adaptive changes in the protein coding regions of brain expressed genes. To this end, we used 454 GS FLX sequencing technology to generate the brain Expressed Sequence Tags (ESTs) of twelve socially diverse bees. The ESTs were assembled into species-specific non-redundant contigs and singletons, which were loaded into a MySQL database using custom scripts. The Honey Bee Homolog Blast website was designed to help users access the database. Users can now download these datasets or BLAST against multiple bee and wasp databases to find the homologues. The results are then sorted by e-value and displayed. The ESTs accessed through the website (http://bee12.cropsci.uiuc.edu ) can be used as a primary tool for gene discovery, genome annotation, and comparative genomic analysis.Since the Honeybee Apis mellifera had its genome recently sequenced, we designed an ortholog identification pipeline that generates multiple sequence alignments of putative orthologous genes across the twelve bees, using the gene models of Apis mellifera as the reference. The evolutionary changes associated with these alignments were then statistically inferred using maximum likelihood methods that make use of sophisticated codon-substitution models to detect non-neutral evolution in the protein coding genes. The rapidly evolving genes were then annotated using gene ontology to find over representation of associated GO terms. We also recently ventured into whole genome sequencing where we generated both single end and paired end whole genome sequence data for two of the bees, Bombus impatiens and Megachile rotundata using Illumina sequencing technology. The reads generated were assembled using a de Bruijn graph based assembly algorithm into scaffolds having a N50 of 1.12 Mb and 31 Kb respectively

data_exp_evol_means_controls

Table containing fertility data for the control populations used to compare with the experimentally evolved populations

Data from: The cost of reinforcement in Drosophila yakuba

When the ranges of two species overlap and the species can hybridize, some individuals may waste gametes on inviable or infertile hybrids. In these cases, enhanced reproductive isolation may evolve as a byproduct of selection against maladaptive hybridization in a process called reinforcement. On the slopes of the African island of São Tomé, Drosophila yakuba and its endemic sister species D. santomea have a well-demarcated hybrid zone. D. yakuba females from within this zone, but not from outside it, show an increase in gametic isolation from males of D. santomea. To understand why reinforced gametic isolation does not spread to the whole geographic range and stays confined to areas of secondary contact, we studied the associated costs of reinforced gametic isolation in D. yakuba by using a combination of natural collections and experimental evolution. We found that D. yakuba males from sympatric populations sire fewer progeny than allopatric males when the female involved in the mating is an allopatric female. The results here shown suggest that the advantageous nature of reinforcement in D. yakuba is local, as its associated costs (i.e., reduced male fertility) might prevent its dispersal outside the hybrid zone

R script used to analyze experimental evolution study

This R script contains code used to analyze fertility at the beginning and end of the experimental evolution component of our study

Comeault_etal_data

Raw data from "Coevolution of male and female reproductive traits and a cascading effect of reinforcement in Drosophila yakuba" Aaron A. Comeault, Aarti Venkat and Daniel R. Matut