CAREER: Ecological Speciation and Heterogeneous Genomic Differentiation in Hybridizing Haplodiploids

Grants and Contracts Details


Ecological speciation—the evolution of reproductive isolation via divergent natural selection—is a major driver of diversification, yet there is still much that we do not know about its genetic underpinnings (Nosil 2012; Schluter and Nosil 2009). When ecological speciation is accompanied by gene flow, genetic differentiation is expected to be highly heterogeneous across the genome, with loci underlying reproductive isolation (RI) exhibiting especially high levels of differentiation (REF). The promise of identifying RI loci without laborious mapping experiments has inspired an explosion of empirical studies documenting genome-wide patterns of genetic differentiation in diverging populations and species. Interpretation of these genomic scans is complicated, however, by the many confounding factors that can shape genomic differentiation (Cruickshank and Hahn 2014). To validate genome scan “outliers” (i.e., putative RI loci) and to test theoretical predictions regarding the genetic architecture of ecological speciation and its influence on genomic landscapes of differentiation, we need to identify relevant loci via independent data (e.g., genetic mapping or selection experiments). Additionally, to determine whether lineages vary predictably in genomic differentiation patterns, it is essential that we conduct genome scans in diverse taxa. For example, haplodiploid sex determination, which has evolved over 20 times and is present in ~15% of all species, is likely to have dramatic consequences for genetic differentiation patterns because all alleles are exposed to selection in haploid males. Yet to date, there are no haplodiploid genome scans. The overarching goal of the proposed work is to understand how divergent natural selection gives rise to reproductive barriers, and how these barriers interact with other features of the genomic landscape and other evolutionary processes to shape genomic differentiation during divergence. To do so, we will focus on a pair of hybridizing haplodiploid sawflies (Neodiprion pinetum and N. lecontei) that are adapted to different pine hosts. We have chosen this species pair because they are experimentally tractable, excellent genomic resources are available, we have confirmed that they exchange genes in the wild, and we have identified divergently selected host-use traits that give rise to RI. To achieve our goals, we propose the following research objectives: 1. To describe the genetic architecture of divergently selected host-use traits, we will map host preference and other host performance traits in the lab. 2. To evaluate the contribution of divergent host preferences to prezygotic isolation, we will conduct trapping experiments in the field to measure habitat isolation. 3. To evaluate the contribution of divergent performance traits to extrinsic postzygotic isolation, we will describe the fitness landscape and map traits and fitness in a field setting. 4. To infer demographic history and describe genome-wide patterns of genetic differentiation, we will re-sequence full genomes of sympatric and allopatric populations of both species. We will interpret these results in light of genome-wide variation in recombination rates, mutation rates, and gene density from existing genomic resources we have developed for Neodiprion. Together, these data will enable us to test theoretical predictions regarding the genetic architectures of adaptation and speciation and their relationship to genome-wide genetic differentiation, as well as evaluate the prediction that divergence-with-gene-flow in haplodiploids produces exceptionally heterogeneous differentiation patterns. To complement this research, we will develop two long-term, self-sustaining integrated research/education/outreach projects: 1. To evaluate spatial and temporal variation in habitat isolation, we will involve members of the local community in trapping efforts and University of Kentucky undergraduates (both majors and non-majors) in PCR-based species identification and hypothesis testing. 2. To describe multifarious agents of selection maintaining species boundaries between hybridizing species, we will involve undergraduates in field experiments that connect genotype, phenotype, fitness, and genetic differentiation. In addition to generating valuable data relevant to my long-term research goals, these integrated research projects will enable us to engage the public, increase scientific literacy in education majors, and promote retention and understanding of evolution in STEM majors
Effective start/end date4/15/183/31/25


  • National Science Foundation: $968,000.00


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