Author ORCID Identifier

https://orcid.org/0000-0002-1911-0344

Date Available

12-3-2024

Year of Publication

2024

Document Type

Doctoral Dissertation

Degree Name

Doctor of Philosophy (PhD)

College

Arts and Sciences

Department/School/Program

Biology

Advisor

Dr. Catherine R. Linnen

Abstract

To explain biodiversity, evolutionary biologists must understand how independent lineages arise via the evolution of reproductive isolation during the speciation process. Hybridizing taxa provide an excellent opportunity to investigate the evolution of reproductive isolating barriers and genomic divergence, thereby enhancing our understanding of speciation. However, hybridization between diverging taxa can vary across geographic space, the genome, and time. Thus, understanding the factors that promote or inhibit hybridization can provide insight into the biotic, environmental, and genetic causes of divergence and gene flow. Importantly, the mechanisms responsible for generating variation in hybridization dynamics and the consequences of such hybridization remains unknown in most hybridizing taxa. In this dissertation, I pose several questions investigating patterns of reproductive isolation, introgression, and divergence at different spatial scales and potential mechanisms generating these patterns in haplodiploid Neodiprion pine sawflies. Neodiprion lecontei and N. pinetum are sister species with large, overlapping ranges and are adapted to Pinus hosts with very different needle morphology. To answer these questions, I combine experimental, morphological, and whole-genome resequencing data from N. lecontei and N. pinetum individuals sampled across both species’ ranges.

In my first chapter, I ask whether body size is a magic trait in N. lecontei and N. pinetum (i.e., under divergent selection and contributes to assortative mating) and whether the strength of prezygotic isolation varies across geographic space. I find that two key requirements for body size to be considered a magic trait are met in N. lecontei and N. pinetum: a large morphological dataset reveals that sawfly adults from populations and species that use thicker-needled pines are consistently larger than those that use thinner-needled pines; fitness data from recombinant backcross females reveal that egg size is under divergent selection between the preferred pines; and mating assays reveal strong size-assortative mating within and between species in three different crosses, with the strongest prezygotic isolation between populations that have the greatest interspecific size differences.

In my second chapter, I characterize patterns of introgression at different spatial scales and time points, test whether human disturbance predicts levels of genome-wide introgression and propose hypotheses about mechanisms that could be causing the patterns I observe. Using a high-coverage whole-genome resequencing dataset from N. lecontei and N. pinetum collected across each species’ range, I find evidence that patterns of introgression vary across geographic space and time points, that genome-wide introgression is higher at sampling locations where average maximum temperature has increased from the 1980’s to the 2010’s, and hypothesize that increasing temperatures have changed hybridization dynamics between N. lecontei and N. pinetum by altering body size and/or phenology.

In my third chapter, I evaluate how the demography and ecology of speciation, haplodiploid transmission genetics and genome features shape the genomic landscape of differentiation between N. lecontei and N. pinetum. Using a low-coverage whole-genome resequencing dataset from N. lecontei and N. pinetum collected in Kentucky, I provide evidence of widespread linked selection across the genomes of N. lecontei and N. pinetum, with genomic predictors of variation differing between the species, and hypothesize that haplodiploid genomes may be heavily influenced by recurrent selection.

In my fourth chapter, I characterize patterns of introgression across the genome for N. lecontei on three different non-native Pinus hosts to test the hypothesis that adaptive introgression can facilitate host shifts in phytophagous insects. Using a high-coverage whole-genome resequencing dataset from N. lecontei and N. pinetum sampled from the Lexington, Kentucky area, I find that, genome-wide, N. lecontei collected on non-native hosts do not have more N. pinetum alleles than N. lecontei collected on native hosts. However, looking at fine-scale patterns of introgression across the genome, I find genomic regions of putative adaptive introgression in N. lecontei on each of the three non-native hosts. Annotation information for genes that overlap with these putative adaptive introgression genomic regions reveal several candidate genes involved in host adaptation. Overall, these findings provide insights into the nature of species boundaries and provide several avenues for future research.

Digital Object Identifier (DOI)

https://doi.org/10.13023/etd.2024.425

Funding Information

This work was supported by the:

  • University of Kentucky Biology Merit Fellowship in 2019
  • University of Kentucky Biology Morgan Fellowship in 2021
  • United States Department of Agriculture (USDA) National Institute of Food and Agriculture (NIFA) Agriculture and Food Research Initiative (AFRI) Predoctoral Fellowship (# 2022-67011-36550) in 2021-2024
  • National Science Foundation (# DEB-1257739)
  • National Science Foundation (# DEB-CAREER-1750946)

Download

Share

COinS