Thursday, 5 May 2022

Evolution News - How the Cephalopods Evolved

The Hawaiian bobtail squid (Euprymna scolopes) is a model system for studying animal-bacterial symbiosis.

Credit: Tom Kleindinst
Squid and Octopus Genome Studies Reveal How Cephalopods’ Unique Traits Evolved | Marine Biological Laboratory

The cephalopods - octopuses, squids and their relatives - are often cited by creationists as something that can't be explained by mainstream evolutionary theory because they, allegedly, have a unique genome. I have even known creationists claim they prove special creation because their favourite creator god created them as a different lifeform. Mind you, I have also known people committed to other wackadoodle notions, claim that they are 'alien' species that arrived on Earth in alien spaceships.

Of course, they are, like all other classes of organisms on Earth, the result of an evolutionary process and there is nothing about their genome that can't be explained in other than standard biogenetic terms. They have exactly the same genetic 'code' as all other life on Earth.

However, that's not to say they don't have some unique characteristics, as these latest papers in Nature Communication show.

As the University of Chicago, Marine Biological Laboratory news release accompanying the two papers explains:

Large and elaborate brains have evolved a couple of times. One famous example is the vertebrates. The other is the soft-bodied cephalopods, which serve as a separate example for how a large and complicated nervous system can be put together. By understanding the cephalopod genome, we can gain insight into the genes that are important in setting up the nervous system, as well as into neuronal function.

Chromosomal-level assemblies allowed us to better refine what genes are there and what their order is, because the genome is less fragmented, so now we can start to study the regulatory elements that may be driving expression of these genes.

Caroline B. Albertin, co-lead author of the first paper.
The Eugene Bell Center for Regenerative Biology and Tissue Engineering
Marine Biological Laboratory
Woods Hole, MA, USA
Squid, octopus, and cuttlefish – even to scientists who study them – are wonderfully weird creatures. Known as the soft-bodied or coleoid cephalopods, they have the largest nervous system of any invertebrate, complex behaviors such as instantaneous camouflage, arms studded with dexterous suckers, and other evolutionarily unique traits.

Probably the greatest advance in this new work is providing chromosomal-level assemblies of no less than three cephalopod genomes, all of which are available for study at the MBL

Professor Clifton W. Ragsdale, co-author
Professor of Neurobiology and of Biology and Anatomy
Department of Neurobiology
University of Chicago, Chicago, IL, USA
Now, scientists have dug into the cephalopod genome to understand how these unusual animals came to be. Along the way, they discovered cephalopod genomes are as weird as the animals are. Scientists from the Marine Biological Laboratory (MBL) in Woods Hole, the University of Vienna, the University of Chicago, the Okinawa Institute of Science and Technology and the University of California, Berkeley, reported their findings in two new studies in Nature Communications.

Comparing the gene content of cephalopod chromosomes allowed us to take the first fundamental steps at deciphering the evolution of cephalopod genomes. The chromosomes and the order of genes in the Nautilus genome, an early-branching group of cephalopods with an external shell and pinhole eye, are comparable to those of other invertebrates. Squid and octopus chromosomes on the other hand look completely different. The chromosomal-level assemblies of their genomes and the comparison of local gene order offer a glimpse at how evolution can take place at the level of DNA, affecting its 3-dimensional organization, gene regulation and likely the appearance and abilities of these intriguing animals.

Hannah Schmidbaur, co-first author
Department of Neuroscience and Developmental Biology
University of Vienna, Vienna, Austria.
The California two-spot octopus, Octopus bimaculoides, was the first octopus genome to be sequenced (in 2015).
Credit: Tom Kleindinst
In Albertin et al., published this week, the team analyzed and compared the genomes of three cephalopod species – two squids (Doryteuthis pealeii and Euprymna scolopes) and an octopus (Octopus bimaculoides).

Sequencing these three cephalopod genomes, never mind comparing them, was a tour de force funded by the Grass Foundation that took place over several years in labs around the world.

The Atlantic longfin inshore squid, Doryteuthis pealeii, has been studied for nearly a century by scientists as a model system for neuroscience investigations.
Credit: Elaine Bearer
In the end, comparing the genomes led the scientists to conclude that evolution of novel traits in soft-bodied cephalopods is mediated, in part, by three factors:
  • massive reorganization of the cephalopod genome early in evolution
  • expansion of particular gene families
  • large-scale editing of messenger RNA molecules, especially in nervous system tissues.
Most strikingly, they found the cephalopod genome “is incredibly churned up,” Albertin said.
In a second paper by scientist led by researchers from MBL, the team found that the genome rearrangements resulted in new interactions that may be involved in making many of the novel cephalopod tissues, including their large, elaborate nervous systems.

Key events in vertebrate evolution, leading to humans, include two rounds of whole-genome duplication. With this new work, we now know that the evolution of soft-bodied cephalopods involved similarly massive genome changes, but the changes are not whole-genome duplications but rather immense genome rearrangements, as if the ancestral genomes were put in a blender.

With this new information, we can begin to ask how large-scale genome changes might underlie those key unique features that cephalopods and vertebrates share, specifically their capacity for large bodies with disproportionately large brains

Professor Clifton W. Ragsdale
The cephalopods' genomes are striking in a number of ways:
  • They are large. The Doryteuthis genome is 1.5 times larger than the human genome, and the octopus genome is 90% the size of a human’s.
  • They’re scrambled. Unlike vertebrates, whose evolutionary history included a couple of instances of whole genome duplication, the cephalopod genomes appear to have been massively rearranged. Not only are they massively rearranged relative to other animals, but they are rearranged relative to one another. It seems these rearrangements created new gene orders an opportunities for evolving large bodies and disproportionately large nervous systems.

Octopus and squid diverged from each other around 300 million years ago, so it makes sense that they seem they have very separate evolutionary histories. This exciting result suggests that the dramatic rearrangements in cephalopod genomes have produced new gene orders that were important in squid and octopus evolution.

An exciting example of that is the protocadherin genes. Cephalopods and vertebrates independently have duplicated their protocadherins, unlike flies and nematodes, which lost this gene family over time. This duplication has resulted in a rich molecular framework that perhaps is involved in the independent evolution of large and complex nervous systems in vertebrates and cephalopods.

Neither of these gene families were found in the octopus. So, these separate groups of animals are coming up with novel gene families to accomplish their novel biology.

Caroline B. Albertin
  • They contain novel gene families.. The team identified hundreds of genes in novel gene families that are unique to cephalopods. While some ancient gene orders common to other animals are preserved in these new cephalopod gene families, the regulation of the genes appears to be very different. Some of these cephalopod-specific gene families are highly expressed in unique cephalopod features, including in the squid brain.
  • Certain gene families are unusually expanded. The team also found species-specific gene family expansions, such as the genes involved in making the squid’s beak or suckers.
  • Prolific RNA 'editing'. The normal process for producing proteins is for the respective section of DNA to be faithfully transcribed into an RNA 'messenger' (mRNA). This mRNA is then transcribed faithfully into a sequence of amino acids in the ribosomes to produce the desired protein. However, this process does not always result in a faithful transcription of the DNA template into protein because the mRNA can be 'edited' to change the sequence of amino acids it codes for. In most of biology, this potential is used very rarely, except in the cephalopods. In an earlier study, scientists from the MBL showed that 60% of mRNA transcripts had been 'edited'. They found 57,000 recoding sites compared to just 100 in humans and 600 in fruit flies. This creates huge opportunity for making novel proteins and represents an alternative to DNA mutations as the basis for natural selection to work on. Instead, natural selection can select for or against novel mRNA editing from the same DNA templates.
The two papers are published open access in Nature Communications:
Abstract

Coleoid cephalopods (squid, cuttlefish, octopus) have the largest nervous system among invertebrates that together with many lineage-specific morphological traits enables complex behaviors. The genomic basis underlying these innovations remains unknown. Using comparative and functional genomics in the model squid Euprymna scolopes, we reveal the unique genomic, topological, and regulatory organization of cephalopod genomes. We show that coleoid cephalopod genomes have been extensively restructured compared to other animals, leading to the emergence of hundreds of tightly linked and evolutionary unique gene clusters (microsyntenies). Such novel microsyntenies correspond to topological compartments with a distinct regulatory structure and contribute to complex expression patterns. In particular, we identify a set of microsyntenies associated with cephalopod innovations (MACIs) broadly enriched in cephalopod nervous system expression. We posit that the emergence of MACIs was instrumental to cephalopod nervous system evolution and propose that microsyntenic profiling will be central to understanding cephalopod innovations.

Abstract

Cephalopods are known for their large nervous systems, complex behaviors and morphological innovations. To investigate the genomic underpinnings of these features, we assembled the chromosomes of the Boston market squid, Doryteuthis (Loligo) pealeii, and the California two-spot octopus, Octopus bimaculoides, and compared them with those of the Hawaiian bobtail squid, Euprymna scolopes. The genomes of the soft-bodied (coleoid) cephalopods are highly rearranged relative to other extant molluscs, indicating an intense, early burst of genome restructuring. The coleoid genomes feature multi-megabase, tandem arrays of genes associated with brain development and cephalopod-specific innovations. We find that a known coleoid hallmark, extensive A-to-I mRNA editing, displays two fundamentally distinct patterns: one exclusive to the nervous system and concentrated in genic sequences, the other widespread and directed toward repetitive elements. We conclude that coleoid novelty is mediated in part by substantial genome reorganization, gene family expansion, and tissue-dependent mRNA editing.

Albertin, C.B., Medina-Ruiz, S., Mitros, T. et al.
Genome and transcriptome mechanisms driving cephalopod evolution.
Nat Commun 13, 2427 (2022). https://doi.org/10.1038/s41467-022-29748-w

Copyright: © 2022 The authors. Published by Springer Nature Ltd.
Open access
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
Although the cephalopods have many unique features in their genomes, such as the evidence of extensive reorganisation in their early evolutionary history, and the extensive use of mRNA editing to modify the genetic 'code' prior to transcription into proteins, these are just variations on a theme common to all DNA-based life forms, and, as creationists might like to note, the scientists who have discovered all this are in no doubt that the present genomes of these cephalopods are the result of perfectly standard evolution.

There is not a hint anywhere in their work to suggest there is some alternative process at work here or that the current Theory of Evolution is inadequate to explain the observable facts. Instead, the TOE is fundamental to their understanding and interpretation of the evidence; without it, none of the facts would make any sense without resort to magical mysteries which tell us nothing of the processes involved and add not one iota to our understanding of the world.

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