Geoffrey Hill, College of Sciences and Mathematics Faculty and Staff

Professional Experience

Innovation

The bright colors, elaborate structures, and extravagant songs and behaviors of animals are among the greatest puzzles in the natural world.  The imperative to explain such traits goes far beyond simply accommodating a curiosity about weird and unexpected phenomena in Nature.  To claim a firm understanding of the process of evolution, biologists must have a well-supported explanation for the evolution of ornaments.  Despite a hundred years of work on the topic, such an explanation has been elusive.

It is now well established that many ornamental traits function in mate attraction, and mate choice can be touted as an explanation for such traits.  However, the bigger question remains: why do females assess such apparently esoteric traits when choosing mates?  Inability to answer this fundamental question haunted Darwin.  In 1860, he famously wrote “The sight of a feather in a peacock’s tail, whenever I gaze at it, makes me sick!”. Why females choose brightly colored males has proven to be formidable question; more than 100 years after Darwin’s death, evolutionary biologists continue grasp for a convincing answer.

My students and I have taken up Darwin’s challenge to understand the evolution of female preferences for male ornaments. After 20 years of investigation and the publication of over 200 refereed journal articles and five books, I proposed a bold new explanation for why females pay attention to male ornaments.  I entitled this new idea the “Mitonuclear Compatibility Hypothesis of Sexual Selection” (reprint attached).  This new hypothesis draws on studies from cell biology and biochemistry to explain male ornaments and to underscore the relevance of sexual selection research to key biomedical topics including aging, metabolic disorders, and cancer.  The gist of this hypothesis is that the greatest imperative for a choosing female is to identify a mate with nuclear genes that are compatible with her mitochondrial genes such that healthy offspring will be produced. This new sexual selection hypothesis builds on discoveries made in the last 25 years that core energy production system of animals, the electron-transport chain in mitochondria, are partly coded for by nuclear genes and partly coded for by mitochondrial genes.  These mitochondrial and nuclear subunits that come together to form the complexes of the electron transport chain must work together in perfect harmony for efficient energy production to be possible.  What I’ve proposed is that ornamental traits are signals of respiratory efficiency such that they enable females to assess mitonuclear compatibility and the likelihood that a male sire will produce vigorous offspring.

The impacts of this discovery will be substantial.  The mitonuclear compatibility hypothesis implicates sexual selection as a primary driver in the evolution of respiratory processes in mitochondria.  A fundamental question in gerontology and oncology is why birds age so slowly and have such low rates of cancer compared to mammals.  For the first time we can propose a comprehensive and coherent answer to this fundamental question: birds are subject to stronger sexual selection that has resulted in better integrated cellular respiration with less production of free radicals which results in less cancer and a slower rate of aging.  Why birds are subjected to stronger sexual selection than mammals is another very fundamental question, and in a recently published commentary in Heredity I’ve proposed that the imperative for females to find complementary nuclear genes is stronger when nuclear genes that express in mitochondria are Z-linked (which indeed they are).

In a nutshell, the ideas developed in my lab group propose that birds are able to sustain high levels of energy production very little leakage of free radicals.  Free radicals damage protein, lipids, and DNA and thus diminish the functionality of an individual.  This accumulated loss of system function is thought to be the basis for both many forms of cancer and aging. Sexual selection has never before been thought of in terms of driving the evolution of better respiratory systems.  The implications are that by studying the outcomes of sexual selection, we can better understand how to avoid the effects of cancer and aging and build therapies based on these new insights. This is an enormous breakthrough in both evolutionary and biomedical sciences.  With the mitonuclear compatibility hypothesis of sexual selection, I have potentially explained female choice for ornaments, resolved the lek paradox, and explained Haldane’s rule. These discoveries emerge from my fascination with the feather coloration and my love of field ornithology.

Studies of plumage coloration in birds and the co-evolution and coadaptation of mitochondrial and nuclear genes has also led Hill to propose new hypotheses for how species form, including most recently to propose a new theory for how prezygotic reproductive isolation evolves. Linking genomic evolution to sexual selection, mate choice, and speciation is an important conceptual advance and hold promise to expand understanding of the origin of biodiversity.