Creationism in Crisis
How Skates' Ability to 'Fly' Through Water Evolved
How Skates' Ability to 'Fly' Through Water Evolved
Adult skate stained with Alcian blue to show the cartilage
© Tetsuya Nakamura
The cartilage of the skate is stained with Alcian blue, the bones with Alizarin red. One of the few places in the world that collects Leucoraja erinacea and breeds it for research, including for the present study, is the Marine Resources Center at the Marine Biology Laboratory in Woods Hole.
© David Gold, Lynn Kee and Meghan Morrissey, MBL Embryology Course
More than 450 million years ago, a primitive fish doubled its genome and so, contrary to creationist fraud claims, doubled the amount of genetic information without the intervention of a magic god. The extra genes were then available to the process of evolution, without loss of function of the original genes, again contrary to creationist claims that all mutations are detrimental, therefore can't be part of evolution.
That doubled genome then drove the evolution of some 60,000 different vertebrates, including mammals such as humans.
Now scientists at the Max Delbrück Center in Berlin, the Andalusian Center for Developmental Biology (CABD) in Seville and other labs have discovered that part of the evolutionary story of skate 'wings' is partly due to the way the DNA containing the genes for them is folded together with the non-coding regulatory sequences that turn thee genes on an off at the right time in the developing embryo.
The major genomic changes to give the skates their 'wings' happened some time ago in its evolutionary history but the main changes since then have been due to changes in this 3D folding.
As the Max Delbrück Center's press release explains:
Genes are not the only drivers of evolution. The iconic fins of skates are caused by changes in the non-coding parts of the genome and its three-dimensional structure, a research team including Darío Lupiáñez at the Max Delbrück Center reports in “Nature”.
The little skate’s dance on the ocean floor is graceful: its massive frontal fins undulate as it skims beneath a layer of sand. With its mottled sand-colored camouflage, the animal is easy to miss.
Scientists at Max Delbrück Center in Berlin, the Andalusian Center for Developmental Biology (CABD) in Seville and other labs have discovered how the skate evolved these cape-like fins by peering into their DNA. They found that the key to the evolution of the skate fins lies not in the coding regions of its genome, but rather in the non-coding bits and the three-dimensional complexes that it folds into. These 3D structures are called “topologically associated domains” (TADs).
The international team describes in “Nature” that genomic changes that alter TADs can drive evolution. Until recently, genome evolution was mostly focused on studying variation at the DNA sequence level, but not in 3D genomic structures. “This is a new way of thinking about how genomes evolve,” says Dr. Darío Lupiáñez, geneticist at the Max Delbrück Center and one of the lead authors of the study.Skate embryo (Leucoraja erinacea) stained with Alcian blue to reveal cartilage.Photo: Elena Boer, MBL Embryology Course
More than 450 million years ago, the genome of a primitive fish — the ancestor of all vertebrate animals — duplicated twice. The expansion in genetic material drove the rapid evolution of more than 60,000 vertebrates, including humans. One of our most distant vertebrate relatives are little skates (Leucoraja erinacea), which belong to a lineage of cartilaginous fishes that includes sharks and rays. These distant cousins are ideal organisms to learn about the evolution of traits that made us human, such as paired appendages.Although we found that unique gene-expression patterns establish exceptionally wide skate fins a while ago, the underlying regulatory changes in the genome have previously remained unknown.
Dr. Tetsuya Nakamura, co-author
Developmental biologist
Rutgers University.
An exciting time in evolutionary genomicsSkates are cartilaginous fishes called Chondrichthyans. They are considered more similar to ancestral vertebrates. We can compare the characteristics of skates with other species and determine what is novel and what is ancestral.
Dr. Christina Paliou, co-first author
Developmental biologist
Andalusian Center for Developmental Biology (CABD)
Seville, Andalusian, Spain
In 2017, the late Dr. José Luis Gómez-Skarmeta from the CABD, a founding figure in evolutionary genomics, brought together scientists from around the world to study skate evolution: laboratories with expertise in genome evolution such as the Ferdinand Marlétaz lab at University College London and Daniel Rokhsar lab at the University of California-Berkeley, in skate biology such as the Neil Shubin lab at University of Chicago, where Tetsuya Nakamura was then located (now at Rutgers) and in 3D gene regulation such as the Juan Tena at CABD, Darío Lupiáñez and Gómez-Skarmeta labs, as well as other collaborators. Gómez-Skarmeta was interested in learning how genomes evolve structurally and functionally to promote the appearance of new traits. “To a great extent, evolution is the history of changing the regulation of gene expression during development,” he said in 2018.
It was an exciting time for evolutionary genomics. Genome sequencing technologies had significantly improved and scientists could gain novel insights into how DNA, which stretches a couple of meters end-to-end, is folded into a 0.002-inch-diameter cell nucleus. “The packaging of DNA in the nucleus is far from random,” says Lupiáñez. The DNA folds into 3D structures called TADs, which contain genes and their regulatory sequences. These 3D structures ensure that the appropriate genes are switched on and off at the right time, in the right cells.
Dr. Rafael Acemel, a geneticist at the Max Delbrück Center and one of the first authors, performed experiments using the Hi-C technology, to elucidate the 3D structure of the TADs. But interpreting the results was challenging at first as the scientists needed the complete skate genome as a reference point. “At the time, the reference consisted of thousands of small unordered pieces of DNA sequence, so that did not help,” Acemel says.
To overcome this difficulty, the scientists used long-read sequencing technology, together with Hi-C data, to assemble the pieces of the DNA like a puzzle and assign the unordered sequences to skate chromosomes. With the new reference, assembling the 3D structure of the TADs using Hi-C became trivial.
They compared this improved skate genome with genomes of the closest relatives, sharks, to identify any TADs altered during skate evolution. These altered TADs included genes of the Wnt/PCP pathway, which is important for the development of fins. There was also a skate-specific variation in a non-coding sequence near the Hox genes, which also regulate fin development. “This specific sequence can activate several Hox genes in the front part of the fins, which does not happen in other fish or four-legged animals,” says Paliou. Subsequently, the scientists performed functional experiments that confirmed these molecular changes helped the skates evolve their unique fins.
TADs drive evolution
Earlier research has shown that changes in TADs can affect the expression of genes and cause diseases in humans. In this study, scientists show a role for TADs in driving evolution that has been previously noted for moles, too.Living embryo of the little skate sitting atop its yolk at approximately ten week.© Mary Colasanto and Emily Mis MBL Embryology Course
After the primitive fish ancestor duplicated its genome, many unused and redundant parts were subsequently lost.
TADs are important for gene regulation, 40 percent of them are conserved in all vertebrates, Acemel says. “However, 60 percent of TADs have evolved in some way or another. What were the consequences of these changes for species evolution? I think that we are just scratching the surface of this exciting phenomenon,” Acemel says.It was not only the genes that disappeared, but also the associated regulatory elements and the TADs they are contained in,” Lupiáñez says. “I think it’s an exciting finding as it suggests that the 3D structure of the genome has an influence on its evolution.
We suspect that these mechanisms might explain many other interesting phenotypes that we observe in nature. By adding these new layers of gene expression, gene regulation, and 3D chromatin organization, the field of evolutionary genomics is entering into a new era of discovery.
Dr. Darío Lupiáñez, co-corresponding author
Epigenetics and Sex Development Group
Max Delbrück Center for Molecular Medicine in the Helmholtz Association (MDC)
Berlin Institute for Medical Systems Biology (BIMSB), Berlin, Germany
This mechanism of evolution constrained by TADs could be prevalent in nature.
The authors give more details in their open access paper in Nature:
Abstract
Skates are cartilaginous fish whose body plan features enlarged wing-like pectoral fins, enabling them to thrive in benthic environments1,2. However, the molecular underpinnings of this unique trait remain unclear. Here we investigate the origin of this phenotypic innovation by developing the little skate Leucoraja erinacea as a genomically enabled model. Analysis of a high-quality chromosome-scale genome sequence for the little skate shows that it preserves many ancestral jawed vertebrate features compared with other sequenced genomes, including numerous ancient microchromosomes. Combining genome comparisons with extensive regulatory datasets in developing fins—including gene expression, chromatin occupancy and three-dimensional conformation—we find skate-specific genomic rearrangements that alter the three-dimensional regulatory landscape of genes that are involved in the planar cell polarity pathway. Functional inhibition of planar cell polarity signalling resulted in a reduction in anterior fin size, confirming that this pathway is a major contributor to batoid fin morphology. We also identified a fin-specific enhancer that interacts with several hoxa genes, consistent with the redeployment of hox gene expression in anterior pectoral fins, and confirmed its potential to activate transcription in the anterior fin using zebrafish reporter assays. Our findings underscore the central role of genome reorganization and regulatory variation in the evolution of phenotypes, shedding light on the molecular origin of an enigmatic trait.
Marlétaz, F., de la Calle-Mustienes, E., Acemel, R.D. et al.
The little skate genome and the evolutionary emergence of wing-like fins.
Nature (2023). https://doi.org/10.1038/s41586-023-05868-1
Copyright: © 2023 The authors.
Published by Springer Nature Ltd. Open access
Reprinted under a Creative Commons Attribution 4.0 International license (CC BY 4.0)
a, Adult little skate (L. erinacea) and skeletal staining using Alcian Blue and Alizarin Red. b, Chronogram showing the branching and divergence time of chondrichthyan and selected osteichthyan lineages (Supplementary Fig. 1). c, Morphological differences in the skeleton between the pectoral fins in shark and skate highlighting the expansion of a wing-like fin. The illustrations were reproduced from a previous publication60. d, Pairwise Hi-C contact density between 40 skate chromosomes, showing an increased interchromosomal interaction between the smallest ones (microchromosomes). The colour scale shows log-transformed observed/expected interchromosomal Hi-C contacts. Macro., macrochromosome; meso., mesochromosome; micro., microchromosome. e, Little skate chromosome classification based on the relationship between their size and GC percentage, highlighting the high GC content of microchromosomes.
And of course, they refute the nonsensical claims by the same creationist frauds that new genetic information can't arise without magic.
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