Research project examines male pregnancy and microbes in fish

A research project from the lab of University of Oregon evolutionary biologist Bill Cresko is setting out to explore the effects of a remarkable evolutionary innovation: male pregnancy in seahorses, pipefish and seadragons.

"This is an amazingly diverse family of fish, and some species are the only vertebrates in which males become truly pregnant," Cresko said "Although male parental care is actually pretty common among vertebrates such as fish - often females will lay the eggs, and it's the males that take care of them, for example in salmon - but it's not clear why this lineage is the only one where the males have evolved pregnancy."

The research is funded through a four-year, $1.6 million grant from the National Science Foundation. Conducted in partnership with the biologist Adam Jones at the University of Idaho, the project is part of the NSF's Rules of Life initiative. Its purpose is to further the understanding of the evolutionary and ecological processes across different scales that produce the range of biological systems across the planet.

This project on syngnathids, the family of 300 or so species that includes seahorses, pipefish and seadragons, will try to answer larger questions about the developmental changes that underly evolutionary innovations. It also will look at the ecological consequences for associated microbiomes, the communities of microorganisms that live inside the animals.

A team of researchers, led by collaborating UO researchers Susie Bassham and Clay Small, will sequence the genomes of syngnathids to better understand some of the genomic changes within the fish that are linked to the evolution of the novel traits they express. That includes not just male pregnancy but also their highly elongated bodies, their lack of pectoral fins and teeth, their elongated snouts and other unusual traits.

Cresko's lab was the first to fully sequence a genome of any fish in this family in 2016.

In order to examine the consequences of evolutionary innovation on the microbial communities associated with the fish, researchers are collaborating with investigators in the lab of biologist Brendan Bohannan, who studies the diversity of microorganisms in environments ranging from the Amazon rainforest to the human gut. Researchers hope to gain a better understanding of how the evolution of novel traits influences the biodiversity of their associated microbial communities.

A working hypothesis of the research team is that the pouches used to brood offspring on the male bodies also evolved to farm the microbes that reduce harmful ones and increase beneficial ones. Previous work in the Cresko lab showed some genes expressed in the pouch likely have effects on microbes.

The central goal of the project is to provide a much more detailed genetic analysis of the development of cells and structures in the syngnathid pouches that might be involved in such 'microbial farming.' In addition to using advanced genomic techniques, such as single-cell sequencing using the UO's advanced equipment in the Genomics and Cell Characterization Core Facility, the team is taking advantage of a recently acquired Xradia microCT imaging system.

The powerful instrument is housed in the Phil and Penny Knight Campus for Accelerating Scientific Impact and was funded by a grant from the M.J. Murdock Charitable Trust that Bob Guldberg, the Robert and Leona DeArmond Executive Director of the Knight Campus, and Cresko secured. It allows researchers to conduct ultra-high resolution 3D scanning and enables virtual dissection of a variety of bony structures in the fish and the specialized male pregnancy cells of seahorses, leafy seadragons and other syngnathids

Bassham has already been working with Angela Lin, a senior research engineer in the Guldberg Lab who is a world expert on those types of microscopes, to acquire stunning images of seahorses and leafy sea dragons. Hope Healey, a graduate student in the Cresko lab studying the evolution of deeply conserved developmental regulatory pathways in syngnathids, also has been a collaborator on the imaging system.

Although the Cresko team's research may eventually inform a better understanding of health and disease, Cresko said the study is a good example of fundamental research that is more focused on gaining knowledge for knowledge's sake. Many such fundamental research projects in years past have led to world-changing applications down the road.

For example, research on microbes in hot springs led to the development of polymerase chain reaction and COVID-19 tests, research into semiconducting materials led to the computer age, and work on microbial "immunity" produced CRISPR technologies that are transforming the treatment of deadly inherited diseases.

"This is science for the joy of understanding the world, because we're human and we're curious and we sometimes just want to discover," Cresko said. "These are simply beautiful and fascinating organisms. Sometimes research is worth doing simply to know how ... in this case, the deep question of how the diversity of life evolves."

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