New Insight Into Primate Eye Evolution

St. Jude study of the nocturnal owl monkey suggests that evolution needed only
a few genetic changes to profoundly alter eye anatomy

MEMPHIS, Tenn., May 18 /PRNewswire-USNewswire/ -- Researchers comparing the
fetal development of the eye of the owl monkey with that of the capuchin
monkey have found that only a minor difference in the timing of cell
proliferation can explain the multiple anatomical differences in the two kinds
of eyes.

The findings help scientists understand how a structure as complex as the eye
could change gradually through evolution, yet remain functional. The findings
also offer a lesson in how seemingly simple genetic changes in the brain and
nervous system could produce the multiple evolutionary changes seen in more
advanced brains, without compromising function.

Analysis for this study was performed at St. Jude Children's Research
Hospital. The primates were housed at the Centro Nacional de Primates in
Brazil. Contributing researchers at Cornell University and Universidade
Federal do Para, Brazil, approved all procedures. The researchers published
their findings in the early online issue of Proceedings of the National
Academy of Sciences.

"The molecular, cellular and genetic pathways that coordinate proliferation
during development have been fine-tuned since the first multicellular
organisms emerged millions of years ago," said Michael Dyer, Ph.D., member of
St. Jude Developmental Neurobiology and the paper's first author. "When these
pathways are deregulated during human development, one of the consequences is
childhood cancer. Therefore, by studying how changes in the regulation of
proliferation during development can lead to dramatic changes in form and
function during evolution, we can gain a deeper understanding of these ancient
pathways that lie at the heart of many pediatric cancers."

The owl monkey's eye has numerous adaptations to make it effective for
nocturnal (active during the night) function. For example, it has a greater
number of rod photoreceptor cells than the capuchin monkey, which is diurnal
(active during the day). Rod cells are the most light-sensitive cells in the
retina making them effective for nighttime vision. The owl monkey's nocturnal
retina is also larger and lacks a fovea, the central region of high-density
cone photoreceptors that gives the diurnal eye high acuity and daytime color
vision.

For both owl and capuchin monkeys, the specialized cell types in the eye all
develop in the growing embryo from a single type of immature cell, called a
retinal progenitor cell.

"These two species evolved about 15 million years ago from a common ancestor
that had a diurnal eye," Dyer said. "So, we believe that comparing how their
eyes develop during embryonic growth could help us understand what
evolutionary changes would be required to evolve from a diurnal to a nocturnal
eye."

The researchers hypothesized that only speeding up or slowing down the
proliferation of the progenitor cells in the developing embryo might actually
change the types of cells that they became. Thus, the evolutionary adaptation
from diurnal to nocturnal eye might require no more than a modest genetic
change that affected that timing.

Such a concept -- that timing of cell proliferation might profoundly affect
anatomy -- has broader implications for understanding how the complex human
brain evolved from simpler mammalian brains, Dyer said. In earlier comparative
studies of the brains of more than 100 mammalian species, the study's first
author, Barbara Finlay, Ph.D., of Cornell University, Ithaca, New York, had
found that those parts of the brain that are disproportionately larger in more
complex brains develop last during embryonic growth.

"This finding suggested that changes in the growth of the brain during
embryonic development could be a mechanism for evolutionary change," Dyer
said. "In other words, maybe the parts of the human brain that are bigger than
in other mammals are bigger simply because the period of their growth is
extended during fetal development."

In their analysis, Dyer and his colleagues compared the timing of retinal
progenitor cell proliferation into the different types of mature retinal cells
in owl and capuchin monkey embryos. They found evidence that the extended
period of progenitor cell proliferation in the owl monkey eye did, indeed,
give rise to the different population of retinal cells that made the eye
specially adapted for nocturnal vision.

They also found evidence that this extended period of proliferation also
caused the size of the eye to be larger, which is necessary for the eye to
accommodate the larger light-gathering and light-sensing structures necessary
for nocturnal vision.

"The beauty of the evolutionary mechanism we have identified is that it
enables the eye to almost toggle back and forth between a nocturnal and a
diurnal structure," Dyer said. "It is an elegant system that gives the eye a
lot of flexibility in terms of specialization."

More broadly, Dyer said, the finding offers support for the idea that
important changes in brain structure can evolve via simple genetic changes
that affect the timing of development of brain regions.

Other authors of this paper are Rodrigo Martins (St. Jude); Manoel da Silva
Filho and Luiz Carlos Silveira (Universidade Federal do Para, Brazil); Jose
Augusto Muniz (Centro Nacional de Primatas, Brazil); and Constance Cepko
(Harvard Medical School).

This research was supported in part by The National Science Foundation.

St. Jude Children's Research Hospital
St. Jude Children's Research Hospital is internationally recognized for its
pioneering work in finding cures and saving children with cancer and other
catastrophic diseases. Founded by late entertainer Danny Thomas and based in
Memphis, Tenn., St. Jude freely shares its discoveries with scientific and
medical communities around the world. No family ever pays for treatments not
covered by insurance, and families without insurance are never asked to pay.
St. Jude is financially supported by ALSAC, its fundraising organization. For
more information, please visit www.stjude.org.

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