Genomic architecture in the Daphnia longispina species complex

Abstract

Hybridization between species across the tree of life is an important evolutionary force that shapes the species’ genomes. The short- and long-term evolutionary consequences of hybridization vary among taxa and are affected by neutral processes, recombination, or selection. The impact of these processes can vary between populations and individuals and lead to diverse outcomes, such as the erosion of reproductive barriers or the introduction of new genetic material for adaptation. The overarching questions addressed in this thesis are about the causes and frequency of recent hybridization in hybrid zones, and how genomic patterns vary among populations and species. I examine these questions in taxa of the zooplankton Daphnia longispina species complex, which is known to hybridize frequently and form freshwater mosaic hybrid zones. To facilitate this, I apply, adapt, and develop appropriate genomic methods to investigate genome-wide hybridization and introgression. Daphnia resting eggs accumulate over time in freshwater ecosystems and are particularly well suited for population genomic studies of hybrid zones and the temporal changes they experience. However, methods were hindered by small amounts of potentially degraded DNA. In Chapter 2, I introduce and test a cost-saving method for whole-genome sequencing of Daphnia resting eggs from the resting egg bank using whole genome amplification and a pre-sequencing contamination screening. This allows us, for the first time, to directly investigate genomic diversity and hybridization in Daphnia populations over several decades. Previous studies of the Daphnia longispina species complex have found frequent hybridization, but lacked a reference genome to characterize genome-wide variability. The D. galeata reference genome I present in Chapter 3, allowed us to identify extensive hybridization and introgression in ecologically diverse habitats. In total, we resequenced and analyzed 49 genomes from the three species and their hybrids, from genotypes sampled in the water column and from single resting eggs extracted from sediment cores. Introgression patterns revealed a complex history reflecting multiple generations of hybridization and backcrossing. Building on this work, I studied the hybridization dynamics of two populations in more detail in Chapter 4. I further improved the reference genome to a chromosome scale and generated more extensive time-series genomic data. Using a novel junctions approach based on how recombination breaks up genomic blocks of contiguous ancestry over time, I demonstrate how it can be used to estimate the extent and timing of hybridization events. I identified recurrent hybridization across the genome over several decades in both populations and diverse genome-wide hybrid ancestry among individuals. These findings establish the Daphnia longispina species complex as a hybrid system with unique features, such as continuous hybridization between multiple species in a mosaic hybrid zone, not previously described in a natural hybrid population. These temporal hybridization dynamics are important to consider as changes to hybrid zones are accelerated by anthropogenic changes in Daphnia and other hybrid systems. Ultimately, I show the temporal dynamics and the diverse genomic landscapes of hybrid individuals with unprecedented resolution. This thesis illustrates the evolutionary complexity required to understand all factors that shape mosaic hybrid zones, such as spatial and temporal changes, recurrent hybridization, and the presence of multiple species.