Jellyfish eye genes suggest a common origin for animal eyes

By Ed Yong | July 27, 2010 8:45 am

Cladomena

Jellyfish may seem like simple blobs but some have surprisingly sophisticated features, including eyes. These are often just light-sensitive pits but species like the root-arm medusa have complex ‘camera’ eyes, with a lens that focuses light onto a retina. Not only are these organs superficially similar to ours, they’re also constructed from the same genetic building blocks.

Hiroshi Suga from the University of Basel has been studying the eyes of the root-arm medusa (Cladonema radiatum). His work strongly suggests that all animal eyes share a common origin, whether they belong to a human or an insect, an octopus or a jellyfish. The details may be different but they’re all under the control of closely related ‘master genes’ that themselves evolved from a common ancestor.

As you might imagine, growing an eye is a complicated business and involves a huge alliance of different genes, switching on and off in a coordinated way. But in humans and other animals, this alliance all comes under the control of a master gene called Pax-6. Pax-6 was discovered in 1994 by Walter Gehring, who also led the current Cladonema study. Faulty copies can cause serious eye problems in animals as diverse as flies and rodents. And activating the gene in the wrong part of the body can produce eyes where they really shouldn’t exist, like the leg of a fly.

Pax-6 is so important that it’s largely the same in very distantly related animals (the technical term is ‘conserved’). You can take the version of Pax-6 from a mouse and shove it into a fly, and it will still be able to trigger the development of an eye. Even though these misplaced eyes have been activated by a mouse gene, they have the compound structure of typical fly eyes. This underlies the role of Pax-6 as a conductor – its job is to coordinate an orchestra of other eye-producing genes.

Pax-6 is just one of a number of closely related Pax genes.  Cladonema doesn’t have a direct equivalent of Pax-6 but it does have three Pax genes of its own, each belonging to a distinct lineage. Only one of these – Pax-A – is actually active in the eyes and Suga clearly showed it’s the jellyfish’s master eye gene. When he transferred it into a fruit fly, he managed to trigger the development of eyes on odd body parts.

Cladonema isn’t the only jellyfish with complex eyes. Another one called Tripedelia belongs to a different group of jellies altogether and it too has a master eye gene called Pax-B, which belongs to a different group to either Pax-A or Pax-6. These three groups of genes evolved shortly after the very dawn of animal evolution from a single ancestral gene that duplicated itself several times. Its copies diverged into the different Pax groups.

So three groups of animals build their eyes using related master eye genes: the hydrozoan jellyfish, represented by Cladonema, use Pax-A; the cubozoan jellies, represented by Tripedelia, use Pax-B; and the bilaterians, including humans and the vast majority of other animals, use Pax-6.

You could argue that this means animal eyes evolved independently at least three times. But Suga disagrees – if this was the case, you might expect the master genes to be recruited from different gene families. As it is, they’re all Pax genes. Instead, Suga thinks that the building blocks of all animal eyes share a common origin. It’s a view that runs counter to the common assertion that animal eyes evolved many times independently but it’s one that Gehring has been championing for years.

When the common ancestor of jellyfish and more complex animals initially evolved eyes, Suga thinks they were under the control of several different Pax genes from the various families. As the bilaterians, hydrozoans and cubozoans diverged from one another, their eye programs eventually fell under the control of single Pax genes from different families. This shared origin explains why genes from one Pax group can still perform the role of genes from the others, and why Cladonema’s Pax-A can produce eyes in a fly.

Eye-evolutionThe evolution of Pax genes. 1) An ancestral gene duplicates itself to produce different classes of Pax genes. 2) The ancestral animal eye evolves under the control of several different classes of Pax genes. 3) In three different animal groups, the Hydrozoa and Cubozoa (both jellyfish) and the Bilateria, eye development comes under the control of species Pax genes. 4) Some of the Pax genes in Bilaterians have been altered.

Reference: PNAS http://dx.doi.org/10.1073/pnas.1008389107


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Comments (9)

  1. Oh no. I just posted a criticism of this same logic about a different trait. Pax genes do more than just regulate eye development. They are found in groups with no eyes and are involved in head formation. They could easily have been co-opted multiple times since they’re expressed in the right place at the right time. It’s not implausible — shared regulatory genes, which have various functions, does not imply homology of structure.

  2. For lots about eye evolution, including the question of how many times they evolved (not really the right question), see:

    Evolution: Education and Outreach

    These aren’t free online anymore, but you can at least find my paper online:

    Gregory, T.R. (2008). The evolution of complex organs. Evolution: Education and Outreach 1: 358-389.

  3. Verbose though it be, here is the relevant bit from my paper on eye evolution under the heading “How many times have eyes evolved?”. I think Todd Oakley made a similar point in his article in the same issue.

    In their classic review of eye diversity and evolution, Salvini-Plawen and Mayr (1977) noted that “it requires little persuasion to become convinced that the lens eye of a vertebrate and the compound eye of an insect are independent evolutionary developments.” Even within a single eye type, for example the camera-type lens eyes of vertebrates versus those of cephalopods, it is obvious that there has been substantial convergent evolution at the level of the organ as a whole. Human and squid eyes are constructed from different tissues, exhibit different morphological organization of the retina and other features, and use different photoreceptors, opsins, and crystallins (Land and Nilsson 2002; Sweeney et al. 2007; Fig. 12). Moreover, the distribution of eyes across the one third of phyla that have them makes it unlikely that they existed in any complex form in the ancestor of all animals because this would require that they have been lost in an improbably large number of lineages (e.g., Land and Nilsson 2002). Similar phylogenetic analyses even suggest that eyes have evolved independently within some taxa (e.g., ostracod crustaceans; Oakley and Cunningham 2002). Thus, considerations of the morphological differences in eyes and photoreceptors and their occurrence in divergent phyla speak strongly in favor of homoplasy. This led Salvini-Plawen and Mayr (1977) to provide an oft-cited estimate in which eyes have evolved independently at least 40 times and perhaps 65 times or more.

    Modern information derived from many lines of evidence, including comparative morphology, molecular biology, phylogenetics, and developmental biology, clearly shows that eyes are the product of a complex evolutionary history. At the same time, the combination of data from these divergent lines of inquiry has tended to blur rather than resolve the long-standing puzzle of how many times eyes have evolved (e.g., Arendt and Wittbrodt 2001; Arendt 2003; Oakley 2003; Fernald 2004a; Nilsson 2004). Whereas “eyes,” strictly defined as complex visual organs, clearly have arisen independently in different lineages, the ancestral opsins and photoreceptors from which all modern eyes are derived are thought to have been present in the last common ancestor of all bilaterians, thereby making them homologous (Arendt and Wittbrodt 2001; Arendt 2003; Fig. 14). It is also possible that vertebrates and jellyfishes inherited their similar opsins and photoreceptors from an even more distant common ancestor, though it has been argued that the intriguing similarities between them reflect independent recruitment of the same genes (i.e., parallel evolution) rather than homology (Kozmik et al. 2008a). The possibility that vertebrate retinal ganglion cells and invertebrate rhabdomeric photoreceptors represent examples of parallel evolution rather than homology also has been raised, though this is not a common interpretation (Nilsson 2004, 2005).

    In any case, most current arguments in favor of eye homology are based not on comparisons of eyes or even photoreceptors, but of genes—specifically, those involved in regulating eye development. In 1994, it was discovered that genes that had been known to cause a loss of eyes when defective in flies (eyeless), mice (small eye), and humans (Aniridia) are, in fact, highly conserved versions of the same regulatory gene: Pax6 (Quiring et al. 1994). The following year, Halder et al. (1995a) manipulated the expression of the eyeless gene in flies so that it was active in tissues other than where it normally functions, with the result that eyes formed on the wings, the legs, and the antennae. Not only this, but Halder et al. (1995a) showed that the Pax6 gene from mice could also induce the generation of eyes in flies—but not mouse eyes, fly eyes (Fig. 15). Similarly, it was shown that ectopic expression of Pax6 would induce the production of eye lenses in non-eye locations in frogs (Altmann et al. 1997; Chow et al. 1999). Observations such as these led to the conclusion that Pax6 is a “master control gene” responsible for eye formation and that it has served this role at least since the last common ancestor of insects and vertebrates. Combined with the notion that photoreceptors also were present in the urbilaterian, it was suggested that “eyes”, defined minimally as a pigment cell and an opsin-containing photoreceptor cell regulated by a version of Pax6, evolved once, with all subsequent eyes arising through tinkering and elaboration of this ancestral system (Halder et al. 1995b; Gehring and Ikeo 1999; Gehring 2001, 2004, 2005; see Kozmik 2008 for discussion).

    It may seem reasonable to conclude, therefore, that eyes simply exhibit deep homology with regard to their underlying photoreceptors, photopigments, and regulatory genes but are homoplasious in terms of their crystallins and overall organization. Life, however, is rarely ever this simple. Thus, it has also been discovered that Pax6 is not the only major gene involved in eye development (in flies, there is a network of seven such genes; Kumar 2001; Gehring 2004, 2005). Moreover, Pax6 is involved in many functions besides eye development, including in brain, nose, and pancreas development in mice. It even regulates some aspects of development in nematodes which lack visual organs altogether (Hodin 2000; Piatigorsky 2008). Therefore, the gene itself may be homologous, but this would not make eyes homologous if its ancestral function was unrelated to the development of visual organs. As Kumar (2001) noted, “several of the eye-specification genes are expressed and are involved in the development of non-eye tissue, but we do not say that the eye is homologous to the brain or to muscles.” It is even possible that Pax6 has been independently recruited for a role in guiding visual organ development in different lineages (i.e., by parallel evolution) because it is one of the few regulatory genes expressed “at the right place at the right time” during development that could be co-opted into this role in each lineage (Hodin 2000).

    Overall, the question of whether “eyes” evolved once or many times remains an open one, though the available answers depend more than anything on definitions and levels of analysis. In fact, it may not be useful to consider complex organs in this way at all. Instead, it is more productive to focus on the components of eyes, which have evolved and been combined and modified in a variety of ways in different groups.

  4. This story reminds of the discovery that segmentation in arthropods and vertebrates is mediated by the same kind of genes, the so-called hox genes

  5. “But Suga disagrees – if this was the case, you might expect the master genes to be recruited from different gene families”
    Not necessarily. Bats, birds and pterosaurs all came up using front legs to fly, instead of say hind legs, independently, because it was the easiest alternative. Similarly, those jellyfish and bilaterians may have independently come to use the same kind of genes for eyes because those genes were the best choice. If you and I separately get lost in the same forest, we may arrive at the same point following the same path simply because it was the easiest
    I am not ruling out Saga’s hypothesis; indeed I am looking forward to hearing of further research into that

  6. David Cameron

    Potentially fantastic on a vinegared rice lump

  7. @Walter,
    A common metaphor that I like is the genetic toolbox, that our toolbox is limited so the same tool gets recruited over and over to do the same job. Similarly, if you choose a wrench when you needed a screwdriver, you probably won’t get the job done as well..

    For what it’s worth, my vote is for convergent evolution…

  8. @ This Scientist:
    yep, good metaphor

  9. doris catchpaw

    I was on the beaches of Prince Edward island where there was a”seemingly’ swarm of jelly fish.one lone one was , or seemed to be staring at me..Is this possible, or was I seeing things??

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