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Biology

The ‘Eyes’ Have It: Co-option of organelles led to the evolution of dinoflagellate eyes

Article: Gavelis, G. S., Hayakawa, S., White, R.A., Gojobori, T., Suttle, C.A., Keeling, P.J., Leander, B.S. 2015. Eye-like ocelloids are built from different endosymbiotically acquired components. Nature. doi:10.1038/nature14593

The eyes are the windows to the soul.

You’re the apple of my eye.

There’s more than meets the eye.

Eyes have always been a provocative organ for people and scientists are no exception – their evolutionary origins are contentious. Eyes are found throughout (and beyond!) the animal kingdom and exhibit a wide diversity in structure and function, from simple photoreceptors (that detect intensity and direction of light) to complex image forming eyes (like those in humans). Within the animal kingdom, we now know that nearly all eyes, despite how simple or complex, have similarities (such as the use of crystallins and opsins) that point to a shared history, extending to a time before vertebrates and invertebrates diverged in the tree of life (Fig 1).

Figure 1. While eyes range in structure throughout the animal kingdom, certain aspects remain the same despite this diversity. Recent discoveries in evolution have found that all eyes (from humans to jellyfish) have crystallins and opsins. These traits are likely from a common ancestor, meaning the evolution of eyes goes back millions of years, possibly to a time before vertebrates and invertebrates split off in the evolutionary tree. Image courtesy of pbs.org.

Figure 1. While eyes range in structure throughout the animal kingdom, certain aspects remain the same despite this diversity. Recent discoveries in evolution have found that all eyes (from humans to jellyfish) have crystallins and opsins. These traits are likely from a common ancestor, meaning the evolution of eyes goes back millions of years, possibly to a time before vertebrates and invertebrates split off in the evolutionary tree. Image courtesy of pbs.org.

The structures in your eye (the cornea, iris, lens, and retina) work in an intricately connected way, which creates an image that is converted to an electrical signal for your brain to process. Even slight alterations in these structures can lead to complete loss of sight. This elaborate organ system, along with other complicated biological structures, has led to a popular intelligent design argument: irreducible complexity. Creationists argue that biological systems like eyes are too intricate to have evolved through a stochastic and gradual process like natural selection. They argue that due to the precise interactions between the structures of the eye, any evolutionarily intermediate eyes would not have functioned, preventing the evolution of a functioning eye.

Fortunately, many evolutionary biologists have proposed numerous viable explanations for the development of complex systems. Irreducible complexity is now widely accepted as pseudoscience and is reject by the scientific community at large. However, irreducible complexity does bring up a good question: how exactly did eyes evolve?

A recent study conducted by a team of researchers at the University of British Columbia developed a compelling argument using, surprisingly, the ‘eyes’ of dinoflagellates. Warnowiid dinoflagellates are a very uncommon group of plankton found throughout the northeastern Pacific Ocean that have an eye-like structure called an ocelloid (Fig 2). Early studies of ocelloids showed an anatomy remarkably similar to animal eyes, containing structures that resembled a cornea, iris, lens, and retinal body. They look so similar to animal eyes that it was even proposed that ocelloids and animal eyes were homologous traits (traits arising from a common ancestor). However, researcher Gregory Gavelis and colleagues, through detailed studies, have found that ocelloids have an extremely unique evolutionary history compared to that of animal eyes.

Figure 2. Light micrographs of three species of Warnowiids (a. Warnowia sp. b. Erythropsidinium sp. c. Nematodinium sp.) used in Gavelis et al.,’s study. Opaque black sports are the ocelloids.

Figure 2. Light micrographs of three species of Warnowiids (a. Warnowia sp. b. Erythropsidinium sp. c. Nematodinium sp.) used in Gavelis et al.,’s study. Opaque black sports are the ocelloids.

Gavelis and company used single cell transmission electron microscopy (TEM) to study the ultrafine structure of the ocelloid and found that the retinal body was made up of interlocking organelles (Fig 3). To further investigate, they dissected the retinal bodies and assessed which genes were active in the organelles. Through careful sequencing of mRNA found in the retinal body, they concluded that it was composed of interlocking structures called plastids (light sensitive organelles, commonly found in plants).

Figure 3. TEM image of a section of the retinal body. The arrow highlights a cellular structure resembling an organelle called a plastid that are interlocked throughout the entire retinal body.

Figure 3. TEM image of a section of the retinal body. The arrow highlights a cellular structure resembling an organelle called a plastid that are interlocked throughout the entire retinal body.

The researchers used focused ion beam scanning electron microscopy (FIB-SEM) to create a 3D model of the ocelloid and found an extensive network of plastids that connect the retinal body to the rest of the cell (Fig 4). Additionally, the FIB-SEM images also revealed a second organelle that was closely associated with the ocelloid. Mitochondria were seen to form a tight sheath around the lens of the ocelloid, forming a cornea-like structure.

whole cell fib

Figure 4. a) TEM image of half of a Warnowiid, showing the nucleus and the ocelloid (highlighted in the white box) b) close up TEM image with overlaid colored FIB-SEM images. Red colors indicates plastid/retinal body and light blue indicates mitochondria/cornea c) FIB-SEM modeled 3D image of the ocelloid, showing the mitochondrial cornea (light blue) surrounding the lens (yellow) connected to the plastid retinal body, which extends through the rest of the cell.

Both mitochondria (which are also present in animal cells) and plastids are endosymbionts. Genetic evidence suggests that millions of years ago, mitochondria and plastids were free-living organisms that were engulfed by other cells. The cells formed a symbiotic relationship, possibly leading to the first eukaryotic organisms. Plastids commonly contain light sensitive pigments and are used in photosynthetic processes while mitochondria are often referred to as the ‘cellular powerhouses’ that generate fuel for the cells to use. However, it seems that in these dinoflagellates, plastids and mitochondria serve a completely different purpose – for sight. This is a perfect example of evolutionary co-option (or exaptation). Co-option is the process of assigning a new function to an existing trait, gene, or behavior and it happens to be one of the best arguments against irreducible complexity. So rather than evolving eyes from scratch, Warnowiids made modifications to pre-existing (complex) organelles, giving them new functions and allowing the development of extremely complicated systems, without the need for non-functional intermediate forms. Sorry creationists.

 This co-option of endosymbionts also illustrates another evolutionary process called convergent evolution. While these ocelloids look extremely similar to animal eyes and may even serve the same function, they evolved from two very different paths. Animal eyes likely evolved by co-opting existing proteins or enzymes, whereas Warnowiid ocelloids evolved by co-opting endosymbionts. By studying convergent traits, scientists can figure out what environmental factors, behaviors, or life history traits drove the evolution of these similar eyes. Thus, these single-celled organisms, who lie pretty far away from us on the tree of life, may illuminate our own evolution.

Ultimately, these discoveries only add a couple more pieces to a still very incomplete puzzle. Very little is known about Warnowiids since they are hard to come by in the environment and are not able to be grown in the lab. And while we now know how their ocelloids evolved, we still don’t know what they use them for. The structures seem to imply that these eyes are image forming, but what do they do with these images? As it turns out, a brain is not a prerequisite for image forming eyes, which only makes it more confusing. What would a dinoflagellate do with an image of their environment? How much could they really see anyways? Until we make more discoveries on the origin and function of eyes, the answer may evade us for a little longer.

Irvin Huang
A recent convert to oceanography, I’m studying under Dr. Anne McElroy at Stony Brook University’s School of Marine and Atmospheric Sciences. My research uses biochemical and genomic methods to investigate how coastal organisms respond to environmental stress.

Discussion

One Response to “The ‘Eyes’ Have It: Co-option of organelles led to the evolution of dinoflagellate eyes”

  1. the real question is how complex is a minimal eye. if a minimal eyespot need only 3 proteins it will be a lot. athe chance to get even one protein is about 10^60:

    http://www.ncbi.nlm.nih.gov/pubmed/15321723

    Posted by gil | August 10, 2015, 2:48 pm

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