Although Dr. Yale Passamaneck, a post-doctoral research fellow working with Dr. Martindale at Kewalo Marine Laboratory, has had a life-long interest in the ocean and the animals that live in it, he didn't grow up dreaming of working on microscopic marine larvae. While growing up in San Francisco, he naturally enjoyed the ocean and its inhabitants -- spending much of his free time exploring tidepools and stalking the latest deliveries of pet store aquariums -- but did not give much thought to what wasn't readily seen with the naked eye. As an undergraduate at University of California Santa Cruz, Dr. Passamaneck focused on flashier fare by training sea lions and dolphins, and performing research SCUBA diving throughout California and in the Aleutian Islands.
But Dr. Passamaneck found his calling when he took a college course in Invertebrate Zoology. "It was amazing to look through the microscope at a rock or piece of algae from the seashore and see it teaming with animals I didn't even know existed. I was fascinated with the diversity and how it had arisen."
From there, Dr. Passamaneck was hooked. He conducted his doctoral research on the evolution of invertebrate animals at Woods Hole Oceanographic Institution, through a program in Biological Oceanography with the Massachusetts Institute of Technology. During a post-doctoral fellowship at Weill Cornell Medical College in New York, Dr. Passamaneck developed his skills as a developmental biologist, investigating the molecular mechanisms underlying notochord formation in the tunicate Ciona intestinalis, one of the closest living relatives of vertebrates.
Now at the Kewalo Marine Lab, Dr. Passamaneck combines his dual backgrounds in invertebrate evolution and developmental biology by investigating the evolution of developmental patterning and the origins of complexity in brachiopods. Brachiopods, or lampshells, first appear in the fossil record in the so-called "Cambrian explosion" over 500 million years ago. Brachiopods were among the most numerous animals on the seafloor for the next 300 million years, until the massive Permian-Triassic extinction event 250 million years ago. As a result, the diversity of brachiopods decreased dramatically, allowing many of the ecological niches they occupied to become dominated by bivalve mollusks such as clams and scallops.
"Brachiopods are a fascinating group of marine invertebrates to work on because so much is known about their evolutionary history from the fossil records, and yet relatively little work has been done on the living animals," noted Dr. Passamaneck. "Even today, paleontologists conduct the majority of brachiopod research and many of them have never seen one alive."
Dr. Passamaneck has been investigating the development of brachiopod larval eyes and how it can inform our understanding of eye evolution. In collaboration with Dr. Andreas Hejnol at the Sars Centre in Bergen, Norway and Dr. Carsten Lüter at the Berlin Museum of Natural History, Dr. Passamaneck has discovered that the eyes of brachiopod larvae are composed of cells similar to those in the eyes of humans and other vertebrates, suggesting that the type of cells used in eyes has changed multiple times over the course of animal evolution.
"Finding these cells in the eyes of brachiopods shows us that eye evolution has been more complex than we had previously thought," said Dr. Passamaneck.
Based upon both the morphology of the cells and the expression of a light-sensitive gene called ciliary opsin, Dr. Passamaneck and his colleagues have been able to establish that the eyes of brachiopods contain ciliary photoreceptor cells, the same type of cells that are responsible for detecting light in the human eye. Although it has been known that animals related to brachiopods, such as annelid worms, have ciliary photoreceptor cells, these cells were thought to be used only for detecting changes in the intensity of ambient light, such as day-night or lunar cycles. The appearance of these cells in the eyes of brachiopod larva, however, suggests that these animals are using these cells to detect the direction light.
More surprising still, Dr. Passamaneck has also found that the ciliary opsin gene, which converts light energy into a chemical signal, is also expressed much earlier in the development of brachiopod embryos, before the formation of any neurons.
"We generally expect to see opsin genes expressed in neurons, which can transmit information about light to other parts of the animal to generate response behavior. To see expression of this gene at a stage of development when we knew that neurons had not yet formed was a bit of a puzzle initially."
In unraveling this puzzle, Dr. Passamaneck and his colleagues now believe that this early ciliary opsin expression may be responsible for the early embryos' ability to move towards light, a behavior they observed while working at the University of Washington's Friday Harbor Laboratories. At these early stages of development, all of the cells on the outside of the embryo have microscopic hair-like structures called cilia, whose beating allows the embryo to move though the water.
"Because the cells expressing opsin are not neurons, we hypothesize that they are acting autonomously, changing the beating of their own cilia in response to light and thus enabling the embryo to move towards light."
Even more remarkable are the potential implications of these findings for our understanding of the evolution of the eye. In "On the Origin of Species", Charles Darwin hypothesized that the earliest stages of eye evolution might have involved non-neuronal cells becoming sensitive to light. And yet, until now, no examples similar to the earliest stages of this process have been identified among bilaterian animals.
Regarding the work, Dr. Passamaneck, said, "This research provides a new model for understanding the very earliest stages of eye evolution, how simple cells on the surface of an animal could become able to respond to light, and how these simple cells could be connected to eventually form something as complex as the human eye. We are very excited to continue with the next phase of this research, investigating the function of the ciliary opsin gene, and how it may be controlling the behavior of the embryo."
Dr. Passamaneck's research on brachiopod photoreceptors is detailed in the research article, "Ciliary photoreceptors in the cerebral eyes of a protostome larva", published online March 1, 2011 in the BioMed Central open access journal EvoDevo (www.evodevojournal.com).