On the Genetic Rules of Interspecific Hybridization

Abstract

Speciation is a process resisting the law of entropy. If genetic information flows freely among different components of the tree of life, the system will collapse into homogeneity. In contrast, each speciation event confines genetic material and creates a nonrandom distribution of matter and information. The tipping point is when lineages still exchange genes, but only in a limited manner due to reproductive isolation. Thus, to understand speciation, we must study how reproductive isolation shapes the flow of genetic information.

In Chapter 1, I study conditions under which speciation is reversible. I develop a theory to investigate how genetic incompatibility collapses under continuing hybridization. I conclude that genetic redundancy can robustly predict collapse dynamics. More redundant incompatibility systems collapse more efficiently, and incompatible alleles can be highly polymorphic within each species.

In Chapter 2, I characterize a novel process of molecular evolution across a butterfly hybrid zone. I show that two Papilio species flanking the hybrid zone have divergent DNA substitution rates. Their molecular clocks tick at different speeds and are mixed between different sides of the hybrid zone, and the strength of mixing provides indirect information about barrier loci. Interestingly, this process significantly decreases the utility of the ABBA-BABA test for introgression.

In Chapter 3, to quantify the randomness of local ancestry in admixture, I develop entropy statistics for ancestry tracts with an arbitrary number of sources. Admixture dynamics under recombination and genetic drift follow entropic laws similar to the second law of thermodynamics. I show that loci associated with reproductive isolation reduce entropy in linked regions. Thus, indirect evidence of reproductive isolation can be inferred from even limited hybrid zone samples.

In Chapter 4, to understand Haldane's Rule in butterflies, I map genomic regions for female sterility and abnormal body size in hybrid Papilio. I find that the Z chromosome controls both traits. I further show that size abnormality can be exactly described by polygenes with identical effects spanning the entire Z chromosome, and that Z-linked recombination often rescues backcross phenotypes. This genetic architecture reveals a highly polygenic basis of Haldane's Rule in female-heterogametic taxa.