Seeing eye to eye – humans, dogs, and squid stare across an evolutionary divide

9 May 2014 by Malcolm Campbell, posted in Biology, Science

Could a greater miracle take place than for us to look through each other's eyes for an instant?” from Walden by Henry David Thoreau (1817-1862)

When he really desires something, our young dog has an uncanny ability to stare you right in the eye. This is his version of a compelling request – the strongest “Please?” imaginable.

Credit: Image by Malcolm M. Campbell.

The young dog’s stare has laser-like intensity. It is directly from his eyes to your eyes. The connection he makes is eerie. And no small wonder why.

When the young dog stares you in the eye, he is staring across a 65-million-year divide. That is the time when the common ancestor of dogs and humans is thought to have wandered the Earth. Using the fossil record, palaeontologists have cast a light back on our distant past, and reconstructed a hypothetical ancestor for all mammals whose females have a placenta – the placental mammals. That ancestor gave rise to all mammal lineages that live on the Earth today – rabbits and deer, bats and whales, dogs and humans alike.

That primordial placental mammal had eyes that we all share today. Each of our eyes is an enclosed structure with an iris and lens, liquid interior, and an image-sensing retina.

While the eye has been a successful evolutionary innovation in our mammalian lineage, it is not a perfect structure. Perhaps its most striking limitation is the way the eye is wired to our nervous system. Rather than having light-sensing cells lining the retina, with neurons sitting behind the retina to transmit signals to the brain, our eyes are constructed outside in. That is, the neurons that connect to the brain are on the inside of the eye – in front of the retina. Consequently, light must pass through the neurons before striking the retina. What’s more, these neurons all gather together on the inside of the eye, then exit as the optic nerve through the retina – leaving us with a blind spot where the nerve exits.

This common, not-quite-optimal construction of the eye is shared by all of our placental mammal kin.  When the young dog stares us in the eye, an eye that shares a common heritage stares back. Despite the time that has passed since we shared an ancestor, our common evolutionary history has bestowed us with very similar tools with which to view the world.

This is not so surprising.

What is more surprising, is that the way our eyes are constructed - the same way dogs’ eyes are constructed – is shared with lineages of animals that are far more distantly related than we are. Recent research shows how evolution works in a very similar manner – fashioning the eye in very distinct animal lineages using an equivalent innovation in the way the genetic code is utilised.

Squid.

Credit: Image by Narchuk, courtesy of Shutterstock. Squid.

Like all organs, the eye is the product of the action of many genes. The majority of those genes provide information about how to make part of the eye. For example, one gene provides information to construct a light-sensitive pigment. Another gene provides information to make a lens.

Most of the genes involved in making the eye read like a parts list – make this or make that. But some genes function to orchestrate the construction of the eye. Rather than providing instructions to make an eye part, these genes provide information about where and when parts need to be constructed and assembled. In keeping with their role in controlling the process of eye formation, these genes are called master control genes.

The most important master control gene implicated in making eyes is called Pax6. The ancestral Pax6 gene likely orchestrated the formation of a very simple eye – merely a collection of light-sensing cells working together to inform a primitive organism of when it was out in the open versus in the dark, or in the shade.

Today, the legacy of that early Pax6 gene lives on in an incredible diversity of organisms, from birds and bees, to shellfish and whales, from dogs to squid to you and me. This means that the Pax6 gene predates the evolutionary diversification of these lineages – during the Cambrian period, some 500 million years ago.

Pax6 genes now direct the formation of an amazing diversity of eye types. Some of these eyes are merely a cup of light-sensing cells. Others are like a pinhole camera, allowing entry of light through a small hole then passing through a hollow cavity to be projected on light-detecting cells to sense an image. Insects have yet another kind of eye, the compound eye, which uses an assemblage of many light-sensing facets to construct an image. Finally, there is the eye that we share with our mammalian kin, the camera eye.

In order to create such an elaborate structure as a camera eye, the complexity of activities that Pax6 had to control increased. To accommodate this complexity, evolution increased the number of instructions that arose from a single Pax6 gene.

Like all genes, the Pax6 gene is an instruction written in DNA code. In order for the code to work, the DNA needs to be read and then copied into a different kind of code. The other code is called RNA.

RNA code is interesting in that it can be edited. One kind of editing removes a piece from the middle of the code, and stitches the two ends together. This is called splicing.

Squid.

Credit: Image by Narchuk, courtesy of Shutterstock. Squid.

The marvel of splicing is that it can be used to produce two different kinds of instructions from the same piece of RNA code. RNA made from the Pax6 gene can be spliced in just such a manner. As a consequence, two different kinds of instructions can be obtained from the same Pax6 RNA. These different versions enable Pax6 to control a greater diversity of genes at different times and in different places during embryo development.

The remarkable innovation provided by Pax6 splicing enables the elaboration of a highly evolved camera eye across all vertebrate lineages – fish, amphibians, reptiles, birds, and mammals.

In recent research, Atsushi Ogura at the Nagahama Institute of Bio-Science and Technology and colleagues found that Pax6 RNA splicing has been used to create a camera eye in a surprising lineage. Pax6 RNA splicing also occurs in the lineage that includes squid, cuttlefish, and octopus – the cephalopods.

Cephalopods have a camera eye with many of the same features as the vertebrate camera eye. Importantly, the cephalopod camera eye arose completely independently from ours. Amongst the pieces of evidence of this independent origin is the fact that the cephalopod eye is wired in a more “logical” fashion than the mammalian eye. That is, cephalopod eye neurons connect to the back of the retina, so that light neither passes through them, nor is a blind spot created by an optic nerve passing through the retina. In some ways, the cephalopod eye is a better version of the camera eye that mammals possess.

The last common ancestor of cephalopods and vertebrates, let alone mammals, existed over 500 million years ago. The camera eye had not yet evolved at that time, and the roles played by Pax6 were much simpler than those needed for a camera eye.

Despite the fact that evolution invented vertebrate and cephalopod eyes independently, and at different times, they both use Pax6 RNA splicing as a means by which to generate more information from one gene. This contrasts with insects, where evolution devised the development of compound eye by duplicating the Pax6 gene, so that new instructions were distributed between the two genes.

The manner in which splicing of the cephalopod Pax6 gene occurs differs from vertebrates. In vertebrates there are two different spliced Pax6 RNA variants. Strikingly, there are five such splicing variants of the cephalopod Pax6 RNA. Each of these variants comes into play at different times during the development of the cephalopod eye. Each cephalopod Pax6 variant presumably exerts control over different suites of genes, at different times, in different places. This is not necessarily because the cephalopod eye is any more complex, it is just a different way of achieving equivalent ends.

Squid.

Credit: Image by Narchuk, courtesy of Shutterstock. Squid.

Cephalopod Pax6 RNA splicing is a wonderful demonstration of how evolution fashions equivalent solutions via entirely different routes. The convergence of eye development in the evolution of squid and humans is akin to the convergence of the bird wing and the bat wing. Using analogous structures, evolution can reinvent innovations that provide advantage to those that bear them.

The young dog’s stare is a reminder of the phenomenal power of the eye – as both a receiver and transmitter of information. We gaze at each other for meaning – to convey information about needs, wants, desires. But there is a deeper meaning there as well. There is a message of our shared heritage, of our common evolutionary origins. And, depending on how recently we shared an ancestor, of the convergent paths we took to reach the same destination.

Note: A much abbreviated and edited version of this post appeared in The Conversation. Much thanks to Akshat Rathi for helping convert it for a more general audience.

Images: All dog photos by Malcolm M. Campbell. All squid photos are courtesy of Shutterstock, through agreement with SciLogs. All squid photos by Narchuk.

References:

Fernald RD (2006) Casting a genetic light on the evolution of eyes. Science 313: 1914-1918

O'Leary MA, Bloch JI, Flynn JJ, Gaudin TJ, Giallombardo A, Giannini NP, & Cirranello AL (2013) The placental mammal ancestor and the post–K-Pg radiation of placentals. Science 339: 662-667

Yoshida MA, & Ogura A (2011) Genetic mechanisms involved in the evolution of the cephalopod camera eye revealed by transcriptomic and developmental studies. BMC Evolutionary Biology 11: 180

Yoshida MA, Yura K, & Ogura A (2014) Cephalopod eye evolution was modulated by the acquisition of Pax-6 splicing variants. Scientific Reports 4, Article number: 4256 doi:10.1038/srep04256
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Dog eye.

Credit: Image by Malcolm M. Campbell. Dog eye.

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