I study evolutionary conflict associated with the divergence and emergence of species, integrating insights from a combination of field, experimental, and comparative genomic approaches. My main interests are in how various genetic conflicts – such as those between the genomes of diverging lineages, different sexes, or the interacting components of the nucleus and mitochondria – get resolved and how this resolution is affected by hybridization. For example, when does hybridization reinforce rather than reduce barriers between diverging lineages? How do sex chromosomes evolve and why do they contribute so greatly and so often to reproductive isolation? To investigate these questions, my research focuses on a species-rich and ecologically, behaviorally, and karyotypically diverse group of songbirds: the estrildid finches (family Estrildidae). Species in this family form numerous natural hybrid zones and many can be kept and crossed in captivity, making this group particularly amenable to the study of speciation and adaptation.

Chromosome inversions and reproductive isolation

The long-tailed finch (Poephila acuticauda) is songbird endemic to the northern tropics of Australia and comprises two hybridizing subspecies that differ in a variety of traits that often contribute to reproductive isolation in birds: bill color, song, sperm morphology, and mitochondrial haplotype. Subspecies also differ with respect to sex-linked chromosomal inversions. While differentiation on the autosomes is minimal, the Z chromosome is home to over 99% of fixed genetic differences between subspecies - many of which are kept in linkage disequilibrium by a ~21Mb inversion. The long-tailed finch is an incredible system with which to examine evolutionary processes related to adaptation and speciation. Ongoing work within the long-tailed finch system examines the genetic and regulatory architecture of carotenoid-based color and sperm morphology variation; as well as the contribution of mitonuclear incompatibilities and chromosomal inversions to reproductive isolation.

In collaboration with Frank Chan, we are currently using a novel approach to non-model linked-read sequence data called ‘Haplotagging’ in order to characterize the chromosome inversions that differentiate hybridizing subspecies of the long-tailed finch, their evolutionary history, and their contribution to reproductive isolation. Working with Simon Griffith and Melissah Rowe, we are nearly finished with assembly and annotation of a de novo reference genome for the long-tailed finch. This new long-tailed finch reference genome will greatly enhance our ability to map structural rearrangement differences between subspecies.

Chromosome inversion evolution in passerines

Why are chromosome inversions so common and why do some taxa have more inversion differences than others? The answer to these questions remain largely enigmatic despite a century of study. Using karyotype records for more than 400 species from 59 families in the most species-rich group of birds (order Passeriformes), I evaluated support for alternative theoretical models of chromosome inversion evolution. These models make contradictory predictions regarding the likelihood of inversion fixation and variance in the speciation history, demography, and ecology of species. In a pair of studies during my PhD with Trevor Price, I found that inversions are common and likely evolving because they are adaptive. Inversions were more common between sympatric and hybridizing sister species than allopatric sister pairs; even controlling for the influence of sister pair age. Inversions were also more common the Z sex chromosome than on the average autosome. The extent of inversion differentiation between passerine species is best predicted by a model in which inversions are selected for during speciation when gene flow occurs before reproductive isolation is complete. 

Genetics of carotenoid-based color variation

Investigating the genetic and physiological basis of traits that differ between populations or species is one of the central aims of evolutionary biology. Many species of birds exhibit dazzling color ornamentation produced by carotenoid pigments (e.g., reds, yellows, and oranges) in their plumage, bills/legs, or retinas. Closely-related species are often distinguished by differences in the presence/absence of these colors. In collaboration with the labs of Simon Griffith and Geoff Hill, I am taking an integrative multi-omic approach to investigate the difference in bill color between hybridizing subspecies of the long-tailed finch: yellow in subspecies acuticauda and red in subspecies hecki. We find that yellow bill coloration is a derived and recessive trait that results from turning off C(4)-oxidation specifically within the bill integument. Bill color variation is in large part due to cis-regulatory divergence in the essential carotenoid ketolation gene CYP2J19 and the enhancer gene TTC39B. We find that yellow-alleles at both loci exhibit signatures of selection favoring their spread and are now the process of introgressing between subspecies. We are actively pursuing the implications of these findings using a variety of comparative ‘omic approaches to better understand carotenoid-based color evolution in this group of finches.

Mitonuclear coevolution - incompatibility dynamics

Mitochondria are essential partners in the lives of bilaterian animals, they generate the energy required for nearly all our cellular activities. To produce energy via oxidative phosphorylation (OXPHOS), proteins from ~150 genes in the nuclear (N) genome must interact directly with mitochondrial (mt) proteins while ~1,200 additional N genes function elsewhere within the mitochondrion. This intimate working relationship is rife with opportunity for conflict. Mitochondria replicate asexually and largely without recombination, leading to mutation rates an order of magnitude greater than that of the nuclear genome. That mitochondria remain functional despite this feature is thought to be due to compensatory co-evolutionary change in the N-mt genes directly engaged in OXPHOS. An active question in evolutionary biology today is how this arms-race like conflict between N and mt genomes within lineages results in N-mt incompatibilities between lineages.

In work led by Kelsie Lopez, for her undergraduate honors thesis at Cornell University, we found that long-tailed finch subspecies are ~1% divergent in their mitochondrial genomes and that geographic overlap of mitochondrial haplotypes in the wild occurs in a narrow geographic region (30 km wide). We observed that mitochondrial and Z chromosome admixture is geographically co-located and note the rarity of one direction of mitonuclear mismatched hybrid. In work led by Callum McDiarmid, as a PhD student in Simon Griffith’s lab, we have pursued the implications of this finding from the wild using high resolution respirometry to quantify differences in aerobic metabolism (OXPHOS) directly in captive bred individuals of each parental subspecies and their hybrid crosses. Ongoing work to examine mitonuclear coevolution/incompatibility dynamics is funded by the Australian Research Council in collaboration with the labs of Dr. Simon Griffith and Dr. Antoine Stier.

The ‘Faster-Z Effect’ in the Australian Grassfinches

Genes on sex chromosomes are well-documented to exhibit faster rates of protein coding evolution relative to those on the autosomes. In birds, this elevated rate of evolution for genes on the Z chromosome is known as the ‘Faster-Z Effect’. Despite empirical evidence suggesting that the phenomenon is widespread across avian taxa the underlying mechanisms responsible for Faster-Z evolution remain a subject of debate. In order to evaluate evidence for the Faster-Z, and assess and magnitude and drivers responsible, I am currently evaluating whole genome sequence data for species from a group known as the Australian grassfinches (family Estrildidae). In this group, Z-linked genes evolve ~1.3X as fast as those on comparable autosomes. Utilizing protein sequence and polymorphism data, I am investigating the relative contributions of selection versus drift in producing the Faster-Z in this group. My results suggest that in the Australian grassfinches, higher rates of evolution for Z-linked genes is explained in large part by the increased efficacy of selection acting on sex chromosomes. This result contrasts markedly with other recent studies highlighting a prominent role for genetic drift in producing the Faster-Z Effect.

Mutation spectrum evolution

Mutation, the root source of genetic variation upon which evolution acts, is itself an evolving process; one governed by the dynamics of the cellular DNA damage and repair machinery. The relative mutation rate of different three-base-pair genomic motifs (e.g., TAC->TGC vs TCC->TAC) varies both between species and between different genomic compartments. The relative contribution to mutation spectrum variation of life history and ecological differences between species remains an open and exciting area of research. In work with Amelia Demery, a PhD student in Irby Lovette’s lab, we are currently investigating mutation spectrum evolution in the family Estrildidae using whole-genome genetic variation in order to identify and describe the mutagenic signatures that i) have evolved to differentiate species and those that ii) are conserved by genomic compartment.