Common genes in vertebrates and invertebrates

Many research studies in the last few decades compared vertebrate DNA to that of cnidarians (sea anemones), cephalochordates (amphioxus), annelid worms, and other animals in order to determine the evolutionary relationships at the base of the animal kingdom. Many genes and gene patterns in vertebrates and other chordates are found in cnidarians and annelids. This indicates a common origin of cnidarians, annelids, and chordates.

Many research papers show color coded diagrams of parallel genes in different organisms such as annelids and vertebrates. Figure 9-17 is one example. The colors in Figure 9‑17 represent identical genes surrounding the vertebrate notochord and the annelid axochord. Genes are expressed in approximately the same positions in vertebrates and annelids even though the dorsal-ventral orientation is inverted, and the annelid genes are surrounding an annelid axochord while the vertebrate genes are surrounding a vertebrate notochord. These types of common gene patterns indicate a close evolutionary relationship between annelid worms and vertebrates. This indicates that the chordates and annelids had already formed and diverged from a common ancestor, or as some have proposed, the ancestral organism of the vertebrates was an annelid worm.

The neurosecretory (control weight gain, metabolism, and reproduction) genes in the annelid worm Platynereis are aligned with vertebrates and modern cephalochordates.[2] Neural networks are constructed by genes called neurotrophins that control the growth and survival of neurons. They specify that nerves form and connect at specific locations. There is similarity in nerve types and neurotrophins between vertebrates, cephalochordates and the annelids.[3] There are many ancient genes that are common to all bilaterians. For example, retinoic acid (RA) governs the activation of genes. The retinoic acid system in vertebrates is similar to but advanced from annelids.[4]

The Pax6 protein triggers eye evolution in both the cephalopod (squid) and the vertebrate but not in arthropods (insects and crustaceans). The annelid worm Platynereis, which has two different types of photoreceptor cells, one of which is found in insects (rhabdomeric compound eyes) and the other (ciliary) is found in deuterostome vertebrates and in squids.[5]

There are several examples of single genes that are found in annelids becoming sets or families of genes in vertebrates with enhanced capabilities. For example, the gene vtg is found in annelids. It is also found in vertebrates as the vtg family of genes.[6]

The process of body formation begins with segmentation genes that define the divisions between body segments and trigger specific homeotic genes that trigger the formation of structures in the segments. Hox genes govern the formation of body plans. Hox genes are homeotic genes. There is one set of Hox genes in invertebrates and four to seven sets of Hox genes in vertebrates. Radially symmetric cnidarians (sea anemones) have three Hox genes that are expressed in the same order as the homologous Hox genes in bilaterians, which is evidence of the descent of all bilaterians from cnidarians.

Hox genes line up in clusters in DNA in the same order with which they trigger the formation of different parts of animals. They create Hox proteins, which bind to DNA sites just prior to the genes that they trigger. As they bind to these sites, they cause the target gene to unwind and manufacture RNA and proteins, which then in turn trigger formation of other proteins. Concentration gradients of these proteins form in developing embryos and instruct each cell as to the type of cell that it will become.

Hox genes are aligned in DNA in the same order in which they are expressed in the body. Nematodes (C. elegans) have 6 Hox genes (first row in Figure 9‑17) that are not closely aligned with those of protostomes and deuterostomes. Hox genes along the body are somewhat aligned between protostomes and vertebrates and closely aligned between cephalochordates and vertebrates. This means that nematodes (pseudocoelomates) diverged from protostomes and deuterostomes (coelomates) prior to the time that protostomes and deuterostomes diverged from each other.

Protostomes generally have one Hox gene cluster with 8 Hox genes (Figure 9‑17). Cephalochordates have one Hox gene cluster with 14 Hox gene positions. Vertebrates have 4 to 7 Hox gene clusters with 14 Hox gene positions, not all of which are filled. There are 4 clusters of Hox genes in land vertebrates, and with the displacement of vertebrates at the base of vertebrates, it seems likely to me that there were 4 sets of Hox clusters in Haikouichthys. Ray finned fish and lampreys have 6 to 7 Hox clusters, but that was probably due to a subsequent duplication of Hox genes. Many scientists have thought that there were two genome duplications that led to the origin of the vertebrates.

Reptiles and mammals descended from lungfish, which are bony fish with muscular fins. The positions of Hox genes in lungfish are close to their positions in mammals (Figure 9‑17). Mammal Hox genes, including humans, include 39 Hox genes arranged in four clusters (HOXA, HOXB, HOXC, HOXD). Of 33 Hox genes in four Hox gene clusters in lobe-finned fish, 32 have analogues in mammals.[7] The lobe-finned fish Hox gene clusters are much closer to mammal Hox genes than those of ray-finned fish. Thus, they are the closest living aquatic relatives of the tetrapods.[8]

Just as there is a one-to-four relationship in Hox gene clusters between amphioxus and vertebrates, there is also a general one-to-four relationship in many gene families. One gene in amphioxus often corresponds with four genes of the same gene family in vertebrates.[9] Scientists generally attribute this increase from one to four to two whole genome duplications (2R WGD). Some scientists have questioned whether the increase in vertebrate complexity and the format of the vertebrate genome can be attributed to two whole genome duplications. For example Hughes argued that two genome duplications would lead to (AB) and (CD), but that the actual structure of the four is generally A and (BCD).[10] Aase-Remedios stated that two whole genome duplications would generally lead to four genes at corresponding locations on four chromosomes, but this is generally not the case. [11]

Although it is a popular concept, it is questionable that two instantaneous whole genome duplications led to the complexity of systems such as the eye and hearing in vertebrates. Genome duplication can explain the origination of families of genes from a single gene, but it does not explain the origination of the completely new families of genes in vertebrates. In general, genome duplication can explain diversification but not origination. Other genome duplication events in the history of life did not lead to increases in morphological complexity.[12] Genome duplication can explain diversity, such as the diversification of bony fish after a genome duplication event later in the history of fish, but it seems unlikely to explain the formation of completely novel sensory organs such as sight, hearing, and smell in vertebrates.

There were not only novel genes in vertebrates, but there were novel molecules. There was an increase in microRNA families at the time of the origin of the vertebrates.

“41 microRNA families evolved at the base of the vertebrata….When placed into temporal context, the rate of miRNA acquisition and the extent of phenotypic evolution are anomalously high early in vertebrate history, far outstripping any other episode in chordate evolution.” [13]

Even though there is generally a four-to-one relationship between some genes in vertebrates compared to invertebrates, this does not mean the entire genome of vertebrates is four times as large. In fact, the vertebrate genome is approximately the same size as the amphioxus genome. Many protostome genomes are much larger than the early fish genomes.

Although genes generally change and mutate and have been adapted for various purposes, the coding regions of Hox genes almost never change. The homeobox is the central 180 deoxyribonucleic acids in a Hox gene (coding region). Patterns in the homeoboxes are conserved because changes in a homeobox result in several mutations in the animal. While mutations could be beneficial in one respect, the problem is that each homeobox controls the development of several different animal body parts. Thus, a beneficial mutation caused by a change in the coding region of a Hox gene is nearly always accompanied by a fatal mutation in some other part of the animal.

The evolution of body plans of fish and land tetrapods was caused by changes in the noncoding regions of Hox genes. Although changes in the coding regions of Hox genes cause death, changes in noncoding regions of Hox genes are common and enable animal body plans to evolve into more competitive forms. This has been the key to the evolution of jawed fish, amphibians, reptiles, mammals, and birds. David Kingsley’s group at Stanford proved that mutations in the noncoding region of the Pitx1 Hox gene (Shapiro et al., 2004; Colosimo et al., 2004; Peichel et al, 2001) caused changes in stickleback anatomy.[14] [15] [16] During the last ice age, the stickleback fish only lived in the ocean, and it had spines on top and armored plates as protection from larger fish in ocean waters. As the ice retreated 10,000 years ago in North America, at the end of the last ice age, stickleback fish entered the lakes of North America. They encountered different predators in freshwater lakes, which grabbed and captured the fish by their spines; thus, the spines that had formerly protected them in the ocean were a liability in the lakes. Likewise, armored plates that protected them in the ocean reduced the speed and maneuverability of sticklebacks and made them more vulnerable to capture in lakes. As a result, over the last 10,000 years, stickleback fish in some North American lakes lost their spines and armored plates. Sequential layers of sediment in lake bottoms show gradual changes in spine length and armor coverage. Similar Hox genes that govern body plans in protostomes and cephalochordates, govern the formation of body plans in vertebrates (Figure 9‑17).

References

[1] Lauri, Antonella, Thibaut Brunet, Mette Handberg-Thorsager, Antje HL Fischer, Oleg Simakov, Patrick RH Steinmetz, Raju Tomer, Philipp J. Keller, and Detlev Arendt. "Development of the annelid axochord: insights into notochord evolution." Science 345, no. 6202 (2014): 1365-1368.

[2] Tessmar-Raible, Kristin, Florian Raible, Foteini Christodoulou, Keren Guy, Martina Rembold, Harald Hausen, and Detlev Arendt. "Conserved sensory-neurosecretory cell types in annelid and fish forebrain: insights into hypothalamus evolution." Cell 129, no. 7 (2007): 1389-1400.

[3] Lauri, Antonella, Paola Bertucci, and Detlev Arendt. "Neurotrophin, p75, and Trk signaling module in the developing nervous system of the marine annelid Platynereis dumerilii." BioMed research international 2016 (2016).

[4] Handberg-Thorsager, Mette, Juliana Gutierrez-Mazariegos, Stefan T. Arold, Eswar Kumar Nadendla, Paola Y. Bertucci, Pierre Germain, Pavel Tomançak et al. "The ancestral retinoic acid receptor was a low-affinity sensor triggering neuronal differentiation." Science Advances 4, no. 2 (2018): eaao1261.

[5] Arendt D., K. Tessmar, M. I. de Campos-Baptista, A. Dorresteijn, and J. Wittbrodt. 2002. Development of pigment-cup eyes in the polychaete Platynereis dumerilii and evolutionary conservation of larval eyes in Bilateria. Development 129(5): 1143–54.

[6] Aruga, Jun, and Minoru Hatayama. "Comparative genomics of the Zic family genes." In Zic family, pp. 3-26. Springer, Singapore, 2018.

[7] Esther Koh, Kevin Lam, Alan Christoffels, Mark Erdmann, Sydney Brenner, and Byrappa Venkatesh. 2003. Hox Gene Clusters in the Indonesian Coelacanth, Latimeria menadoensis, Proceedings of the National Academy of Sciences, 100 (2003), no. 3: 1084-1088.

[8] Ying Cao, Peter Waddell. Norihiro Okada, and Masami Hasegawa,1998. The Complete Mitochondrial DNA Sequence of the Shark Mustelus manazo: Evaluating Rooting Contradictions to Living Bony Vertebrates, Mol Biol Evol, 15 (1998) no. 12: 1637-46.

[9] Aase-Remedios, Madeline, Clara Coll-Llado, and David Ferrier, “More than one-to-four via 2R: Evidence of an independent amphioxus expansion and two-gene ancestral vertebrate state for MyoD-related myogenic regulatory factors (MRFs). Mol Biol Evol. Msaa 147.

[10] Hughes, Austin L. “Phylogenies of developmentally important proteins do not support the hypothesis of two rounds of genome duplication early in vertebrate history.” Journal of molecular evolution 48, no. 5 (1999): 565-576

[11] Aase-Remedios, 2R

[12] Heimberg, Alysha M., Lorenzo F. Sempere, Vanessa N. Moy, Philip CJ Donoghue, and Kevin J. Peterson. "MicroRNAs and the advent of vertebrate morphological complexity." Proceedings of the National Academy of Sciences 105, no. 8 (2008): 2946-2950.

[13] Heimberg, Complexity

[14] Shapiro M. D., M. E. Marks, C. L. Peichel, B. K. Blackman, K. S. Nereng, B. Jonsson, D. Schluter, D. M. Kingsley. 2004. Genetic and developmental basis of evolutionary pelvic reduction in threespine sticklebacks. Nature 439(7079): 1014.

[15] Colosimo P. F., C. L. Peichel, K. Nereng, B. K. Blackman, M. D. Shapiro, D. Schluter, D. M. Kingsley. 2004. The genetic architecture of parallel armor plate reduction in threespine sticklebacks. PLoS Biol. 2(5): E109.

[16] Peichel C. L., K. S. Nereng, K. A. Ohgi, B. L. Cole, P. F. Colosimo, C. A. Buerkle, D. Schluter, D. M. Kingsley. 2001. The genetic architecture of divergence between threespine stickleback species. Science 414(6866): 901–5.

Banner

Piece of DNA being removed by tweezers. Credit: Ciencias Españolas KoS . Used here per CC BY-SA 3.0.