Research shows Darwinism in action

An ovary of the live-bearing placental fish, Poeciliopsis prolifica. At image center is a late stage embryo with the network of blood vessels of the placenta. In the background are a one-cell embryo and embryos at earlier stages. Image courtesy of Michael O’Neill.

UConn scientists and collaborators at other universities have found experimental evidence that supports a controversial theory of genetic conflict in the reproduction of animals that support their developing offspring through a placenta.

The conflict has been likened to a “battle of the sexes” or an “arms race” at the molecular level between mothers and fathers. At stake is the fetus’s growth rate and how much that costs the mother, who supplies its nutrients.

The new research, led by Michael O’Neill, associate professor of molecular and cell biology in the College of Liberal Arts and Sciences at UConn, supports the idea of a genetic “arms race” going on between a live-bearing mother and her offspring, abetted by the growth-promoting genes of the father.

The research provides a rare example of Darwinism in action at both the DNA and the species levels.

It is described in a new paper, the cover story of the July 24 issue of the scientific journal, Proceedings of the National Academy of Sciences.

The paper was one of PNAS’s top 20 most-read papers online during July.

Michael O’Neill is the lead author. Rachel O’Neill, associate professor of molecular and cell biology, faculty from other institutions, and graduate students from UConn and elsewhere are co-authors.

The O’Neills, who are married to each other, are active researchers at UConn who often hold joint meetings of their research groups and collaborate on projects.

The paper was edited by Shirley M. Tilghman, president of Princeton University and a molecular biologist with a particular interest in this area of study. She was Michael O’Neill’s postdoctoral adviser.

Part of the significance of the research is in providing experimental proof of a theory put forth in the 1990s by Harvard University biologist David Haig and others.
It holds that in animals with a placenta, genetic material from the father and the mother promote different growth rates in the embryo, which produces a conflict over nutrients.

The genetic material from the father is hard-wired to provide fast fetal growth, so that his offspring will be the hardiest, best survivors, the ones who demand the most of the mother’s placental nutrients.

The mother, on the other hand, provides genetic material that promotes the same growth level for all of her offspring, so that her nutrients will be available to support her and the offspring from all her matings.

So the initial skirmish in the battle of the sexes could be said to take place at the embryonic level. Whose genetic material will prevail in the offspring, and which offspring will prevail in the survival of the species?

Evidence to support the “parent-offspring conflict theory” has been found in placental mammals. But the O’Neill study is the first to look for this conflict in any of the many species other than mammals that have evolved placental reproduction.

The CLAS scientists and their collaborators studied a family of livebearing fish that includes the popular aquarium species of mollies and guppies. Most fishes are egg-layers, but some species in this family have evolved a placenta-like structure and give live birth.

The new research tested the conflict theory by studying samples of the IGF2 growth hormone (insulin growth factor 2) collected from 50 species of minnows. The IGF2 gene is found in all vertebrates, including fish and people. It is the primary fetal development growth hormone.

The IGF2 gene sequences looked different in some species of the minnows, showing that segments of the gene had evolved. It appeared that the biggest changes were in those species of the minnows that had developed placentas.

Michael and Rachel O'Neill. Photo by Daniel Buttrey.

The question for the researchers was, did the changes they saw in the IGF2 gene sequence exactly correlate with the evolution of the placenta? Was there a cause and effect, or was the change just random?

A random change would be from DNA mutating, which occurs all the time.

The researchers found instead that the change they saw supported the Darwinian theory of natural selection, providing independent support for the theory of conflict between the male and female genetic material in producing offspring.

The genomes of placental animals are fundamentally affected by being placental, and it is the imbalance of parental investment in the offspring, or the battle of the sexes at the molecular level, that changes the genome, the researchers found.

“It’s very rare to find good examples of Darwinian selection,” said Rachel O’Neill, “but we can definitely say it is placental, and that has led to Darwinian selection.”

Usually, Darwinian selection is inferred from the diversity of species and observation of how animals have adapted, she noted.

About 50 species of minnows were used in the new study. A population of desert top minnows has been maintained at UConn for research for several years. Additional research specimens were provided by co-author David N. Reznick from the University of California-Riverside, a leading authority on live-bearing fishes. Other fish species were provided by co-author Mariana Mateos at Texas A & M University and by co-author Tomas Hrbek of the University of Puerto Rico-Rio Piedras.

Detailed statistical analysis of the findings was done by Dawn M. Carone and Gianni C. Ferreri, PhD students advised by Rachel O’Neill, using a large array of parallel computers in UConn’s Biotechnology Center. The computer power made it possible to analyze data in hours rather than days, Michael O’Neill noted.

The research project was funded in part by the National Science Foundation, with additional funding from the University of Connecticut Research Foundation and support from the College of Liberal Arts and Sciences.