Hox cluster found in Crown of Thorns starfish a surprise

A Crown of Thorns starfish, Acanthaster planci, feeding on several species of Montipora corals. The image was taken off the coast of Okinawa near Sesoko Island. Credit: Yuna Zayasu

New research published in the journal genesis, by Kenneth Baughman, Dr. Eiichi Shoguchi, Professor Noriyuki Satoh of the Marine Genomics Unit at the Okinawa Institute of Science and Technology Graduate University, and collaborators from Australia, reports an intact Hox cluster in the Crown of Thorns starfish, Acanthaster planci. This surprising result contrasts with the relatively disorganized Hox cluster found in sea urchins, which are also echinoderms, classification of animals including starfish, sea lilies, and sea cucumbers. Stanford University Professor Christopher Lowe, who studies developmental biology in echinoderms, summarizes the paper: "The translocation of the Hox cluster in echinoderms has been a major red herring for understanding their evolution. It's really good to have some hard data showing that some echinoderms exhibit some oddities that are not representative of all echinoderms."

The Hox cluster is a classic example of an 'evo-devo' genetic toolkit. The term "evo-devo" refers to the study of genetic programs that control development, which can be compared between species, and thus, across evolutionary time. 

The Hox genes coordinate segmental identity along the head to tail (anterior-posterior) axis. The Hox cluster is evolutionarily conserved and has been 

repurposed repeatedly during the evolution of the animal body plan, or how animals are shaped. Past studies have shown that Hox clusters organize the development of brain and central nervous system regions in chordates, limb bud identity in vertebrates, and, classically, antennae or wing segment identity in fruit flies.

Generally, the Hox cluster shows "colinearity," in which gene order correlates with the location of expression, or the developmental stage of expression. "For example, anterior Hox genes are expressed in regions that are closer to the head of an embryo, and are expressed sooner during development, versus the posterior Hox genes," explained Baughman. "Thus, we were surprised to see chordate-like Hox cluster organization in starfish, which have a radial body plan." Echinoderms are classical model organisms for embryology, and more recently evo-devo. Baughman added, "Interacting with the speakers and students of theOIST Winter Course 'Evolution of Complex Systems' (OWECS) allowed me to appreciate the importance of finding an intact Hox cluster in starfish."

The Crown of Thorns starfish, a predatory starfish which feeds on corals, is famous for its dramatic changes in population density on the reefs near Australia, as well as Okinawa. Over the past 50 years, this has resulted in a measurable loss of coral reefs. A recent 27-year reef monitoring study of the Great Barrier Reef estimated that the starfish accounts for 42% of the loss in coral cover, 2nd only to typhoons. While population control was the initial motivation for Crown of Thorns genome research, the Hox cluster report is one of the first to show that the species can be useful for studies in evolutionary-developmental biology. "We were excited to see the entire Hox cluster on a single genomic scaffold, a result which confirmed the remarkably high quality of the genomic data," said Prof. Satoh.

As is often the case with science, the discovery raises more questions than it answers. If starfish have a collinear Hox cluster, what accounts for their dramatic departures in body plan organization? Do starfish express Hox genes during development in a manner similar to chordates, as indicated by the organization of their Hox cluster? Baughman looks forward to addressing these questions and many more as part of his doctoral research. "I look forward to pursuing developmental biology studies that may suggest methods for mitigating damage to the coral reef caused by the Crown of Thorns starfish."

More research is being conducted at OIST on the Crown of Thorns starfish in the Marine Biophysics Unit by Masako Nakamura in cooperation with local fishermen. In addition to the research collaboration highlighted by the Hox publication, recent efforts by the Okinawa Prefectural Government and Australian Institute of Marine Science are also working on projects to protect the existing coral reefs from the Crown of Thorns starfish.

Source: Okinawa Institute of Science and Technology - OIST

A clear, molecular view of how human color vision evolved

Mountain Gorilla - Bwindi Uganda. “Gorillas and chimpanzees have human color vision,” Yokoyama says. “Or perhaps we should say that humans have gorilla and chimpanzee vision.” Credit: © Alexander / Fotolia

Many genetic mutations in visual pigments, spread over millions of years, were required for humans to evolve from a primitive mammal with a dim, shadowy view of the world into a greater ape able to see all the colors in a rainbow.

Now, after more than two decades of painstaking research, scientists have finished a detailed and complete picture of the evolution of human color vision. PLOS Genetics published the final pieces of this picture: The process for how humans switched from ultraviolet (UV) vision to violet vision, or the ability to see blue light.

"We have now traced all of the evolutionary pathways, going back 90 million years, that led to human color vision," says lead author Shozo Yokoyama, a biologist at Emory University. 

"We've clarified these molecular pathways at the chemical level, the genetic level and the functional level."

Co-authors of the PLOS Genetics paper include Emory biologists Jinyi Xing, Yang Liu and Davide Faggionato; Syracuse University biologist William Starmer; and Ahmet Altun, a chemist and former post-doc at Emory who is now at Fatih University in Istanbul, Turkey.

Yokoyama and various collaborators over the years have teased out secrets of the adaptive evolution of vision in humans and other vertebrates by studying ancestral molecules. The lengthy process involves first estimating and synthesizing ancestral proteins and pigments of a species, then conducting experiments on them. The technique combines microbiology with theoretical computation, biophysics, quantum chemistry and genetic engineering.

Five classes of opsin genes encode visual pigments for dim-light and color vision. Bits and pieces of the opsin genes change and vision adapts as the environment of a species changes.

Around 90 million years ago, our primitive mammalian ancestors were nocturnal and had UV-sensitive and red-sensitive color, giving them a bi-chromatic view of the world. By around 30 million years ago, our ancestors had evolved four classes of opsin genes, giving them the ability to see the full-color spectrum of visible light, except for UV.

"Gorillas and chimpanzees have human color vision," Yokoyama says. "Or perhaps we should say that humans have gorilla and chimpanzee vision."

For the PLOS Genetics paper, the researchers focused on the seven genetic mutations involved in losing UV vision and achieving the current function of a blue-sensitive pigment. 

They traced this progression from 90-to-30 million years ago.

The researchers identified 5,040 possible pathways for the amino acid changes required to bring about the genetic changes. "We did experiments for every one of these 5,040 possibilities," Yokoyama says. "We found that of the seven genetic changes required, each of them individually has no effect. It is only when several of the changes combine in a particular order that the evolutionary pathway can be completed."

In other words, just as an animal's external environment drives natural selection, so do changes in the animal's molecular environment.

In previous research, Yokoyama showed how the scabbardfish, which today spends much of its life at depths of 25 to 100 meters, needed just one genetic mutation to switch from UV to blue-light vision. Human ancestors, however, needed seven changes and these changes were spread over millions of years. "The evolution for our ancestors' vision was very slow, compared to this fish, probably because their environment changed much more slowly," 
Yokoyama says.

About 80 percent of the 5,040 pathways the researchers traced stopped in the middle, because a protein became non-functional. Chemist Ahmet Altun solved the mystery of why the protein got knocked out. It needs water to function, and if one mutation occurs before the other, it blocks the two water channels extending through the vision pigment's membrane.

"The remaining 20 percent of the pathways remained possible pathways, but our ancestors used only one," Yokoyama says. "We identified that path."

In 1990, Yokoyama identified the three specific amino acid changes that led to human ancestors developing a green-sensitive pigment. In 2008, he led an effort to construct the most extensive evolutionary tree for dim-light vision, including animals from eels to humans. At key branches of the tree, Yokoyama's lab engineered ancestral gene functions, in order to connect changes in the living environment to the molecular changes.

The PLOS Genetics paper completes the project for the evolution of human color vision. "We have no more ambiguities, down to the level of the expression of amino acids, for the mechanisms involved in this evolutionary pathway," Yokoyama says.

Source: Emory Health Sciences