Saturday, December 31, 2016

Fish Genomes of 2016 in Review

Biology has been booming with rapid advances in DNA sequencing, and now scientists are able to rapidly map out genomes for more and more species. Genes are the basis of many traits, and so sequencing and comparing genomes can help us understand how these genes differ between species to drive their differences in traits, just as comparing genomes of people with a genetic disorder can help identify what gene or genes are involved. Genes also allow us to reconstruct relationships between species. Knowing the genome sequences of other species hence provides many scientific opportunities to understand their biology, and our own biology.

Fish genomics has come a long way since the initial sequencing of the first few fish genomes: zebrafish, pufferfish, and Japanese ricefish (medaka), which began over a decade ago. Fishes are vertebrates just like humans, so we share many biological characteristics with fish. This means fish can provide information on the origins of human genes, and the structure and function of the human genome. Fish genomes can also empower breeders in aquaculture who may be interested in selecting for traits such as faster growth. And of course, sequencing fish genomes can allow us to understand the genetic make-up of fishes that give different species their unique traits. In 2016, we've seen a rapid increase in the number of fish genomes that have been made available*, and here is a list of the last year and a few of their highlighted findings.

Sinocyclocheilus spp.
Sinocyclocheilus anshuiensis, a cave-obligate fish, labeled
with numerous genetic changes involved in adapting to caves.
Src: Yang et al. 2016

The Chinese barbs of the genus Sinocyclocheilus include many species endemic to China, some of which have entered caves and adapted to cave life. Genetic differences between surface Sinocyclocheilus and cave-adapted Sinocyclocheilus may be involved in adaptation to cave life. This is only the second cave-adapted species that has had its genome sequenced (the first being the Mexican cave tetra, Astyanax mexicanus, published in 2014). Chinese cave barbs and Mexican cave tetras show many similar genetic changes compared to surface fish, such as many genes involved in vision, which is usually lost in the perpetual darkness of caves.

Source. doi:10.1186/s12915-015-0223-4

Turbot, Scophthalmus maximus

Turbot, by © Hans Hillewaert /, CC BY-SA 3.0, Link.
Prior to 2016, only one flatfish had been previously sequenced, the Chinese tongue sole, Cynoglossus semilaevis, in 2014. As a popular food fish, the turbot genome will be important for breeding programs, and the genome sequence helped to study the genetics of body growth, sex determination, and disease resistance, which are important traits in fish culture. They also found certain genes related to vision and fat that may be evidence of adaptation to dark and cold water that it would live in on the ocean floor.

Source. doi: 10.1093/dnares/dsw007

Miiuy croaker, Miichthys miiuy

The miiuy croaker is a species of croaker found in waters of China, Korea, and Japan. These fish appear to be relatively poorly studied, and there's not even a freely available image of this species to use here. Of course, they are economically important and used in aquaculture, hence the authors here focus on genes related to their immune system, and found reduced numbers of adaptive immunity genes but expanded numbers of innate immunity genes compared to many other fishes, and they argue that the innate immunity is robust and compensates for the reduction in adaptive immunity. They also find loss of vision genes related to muddy habitats. The authors also found expansions in genes to taste umami which may be related to its carnivorous diet, and that this phenomenon was replicated in other carnivorous teleosts compared to omnivorous teleosts. Finally, genes related to the sense of smell are also in higher number than in most other fishes.

Source. doi: 10.1038/srep21902

Spotted gar, Lepisosteus oculatus

Spotted gar by By Tino Strauss, CC BY-SA 3.0, Link.
The spotted gar genome is an important new addition to the growing genome menagerie. The spotted gar is the first fish genome sequence of a ray-finned fish that is not a teleost. Almost all ray-finned fishes are teleosts. Teleost fishes arose after their genomes duplicated, so many species (such as model organisms like zebrafish) have two copies of many gene when compared to humans. This makes comparisons between humans and ray-finned fishes more difficult. Since the spotted gar is not a teleost, its genome does not contain this duplication, and thus the new genome sequence helps to form a bridge between fish and human genomics.

Source. doi: 10.1038/ng.3526

Asian seabass, Lates calcarifer

Asian seabass, CC BY 2.5, Link.
The Asian seabass is a large, predatory fish that is an important food source in Southeast Asia. With a broad geographic range from northwestern India stretching all the way to Australia, genetic comparisons of the Asian seabass showed that there are three major populations across its range. Furthermore, while many genomes are highly fragmented (and thus are incompletely assembled), this project combined numerous data sources (e.g. long read sequencing, optical mapping, transcriptome scaffolding) to make this assembly one of the most complete among all fishes, which will be useful for chromosome-level genome comparisons.

Source. doi: 10.1371/journal.pgen.1005954

Atlantic salmon, Salmo salar

Atlantic salmon, by By Hans-Petter Fjeld, CC BY-SA 2.5, Link.
The Atlantic salmon is one of the most important fishery species in the Atlantic. Salmon are teleosts, but have another genome duplication of their own that happened after the first teleost genome duplication, so they have quadruple the number of genes. The salmon genome can help us understand how a genome evolves after a recent genome duplication. Having two copies of a gene may not be necessary, so new copies can be lost, evolve new functions, or the two copies can divide their labor and split their roles. The authors of the study found that most new genes that were retained evolved new roles rather than splitting their roles. The Atlantic salmon is the second salmonid genome sequenced, after the rainbow trout Oncorhynchus mykiss, 2014.

Source. doi: 10.1038/nature17164

Asian Arowana, Scleropages formosus (Again!)

Golden, red, and green morphs of Asian Arowana.
Src: Bian et al. 2016 Link.
The Asian arowana is one of the most highly prized ornamental fishes, as documented in a new book The Dragon Behind The Glass. Sometimes called dragonfish, they are prized for bringing good luck and fortune, and are the most expensive ornamental fish. Hence, it is not surprising that multiple teams were sequencing the Asian Arowana genome, and the first genome sequence was published last year. The species comes in multiple color morphs, and the new paper presents genome sequences for golden, red, and green varieties. The scientists report that eels and bonytongues (the group that arowana belongs to) are each others' closest relatives, that they have found two genes that may play a role in golden coloration, and they find arowana may have ZZ/ZW sex determination (information which may allow breeders to determine the sex of fishes when they are young).

Source. doi: 10.1038/srep24501

Channel Catfish, Ictalurus punctatus

Channel catfish, By U.S. Fish and Wildlife Service. Link.
The channel catfish is the most popular aquaculture catfish species in North America, and this genome sequence will be useful for selective breeding for certain catfish traits. In addition, like all other catfishes, the channel catfish does not have scales. Comparisons of the channel catfish with armored catfishes, as well as comparisons between scaled and naked carps, were used to identify a number of genes related to developing scales and armor in carps and catfishes.

Source. doi: 10.1038/ncomms11757

Mangrove killifish, Kryptolebias marmoratus

Mangrove Killifish, Public Domain.
Unlike most vertebrates, the mangrove killifish is a hermaphroditic, self-fertilizing species. The authors found no unusual changes to the sequences of its sex-determining genes, suggesting gene expression changes may be more important to how these fish evolved to be hermaphrodites. This fish is also extremely tolerant of stressful conditions, and is able to breathe air and hop short distances on land. Future work studying its tolerance will be helped by the newly available genome.

Source. doi: 10.1093/gbe/evw145

Ocean sunfish, Mola mola

Ocean sunfish, by By Per-Ola Norman, Public Domain. Link.
The ocean sunfish is the largest bony fish, and can weigh over two tons. To reach its large size, it has a fast growth rate and a relatively light skeleton that is mostly made of cartilage. The authors of the study found that genes related to growth and bone development have undergone positive selection or rapid evolution, which provides evidence that changes to these genes may have evolved that contribute to its large size. The ocean sunfish is also interesting because it lacks a true tail. Hox genes are well known for determining regions of the body, but the ocean sunfish has apparently not lost any hox genes that might explain the loss of its tail, suggesting some other mechanism determines the lack of its tail.

Source. doi: 10.1186/s13742-016-0144-3

Blacktail butterflyfish, Chaetodon austriacus

Blacktail butterflyfish, by Bernd, CC BY-SA 2.0, Link.
The blacktail butterflyfish represents the first tropical coral reef fish genome sequence published (well, accepted for publication). This genome sequence will be useful in future studies of coral reef fish adaptation, evolution of fishes in the Red Sea, and may eventually help with marine aquaculture of coral reef fishes.

Source. doi: 10.1111/1755-0998.12588

American eel, Anguila rostrata

American eel, By Clinton & Charles Robertson, CC BY 2.0, Link.
The publication of the American eel genome follows the publication of the European eel Anguilla anguilla and Japanese eel Anguilla japonica. Given the rapid improvements in genome sequencing and assembly, it also is the highest quality genome assembly of all eels and relatives. This genome will also be useful for future studies on freshwater eels, including conservation genetics and functional genomic studies.

Link. doi: 10.1111/1755-0998.12608

Japanese flounder, Paralichthys olivaceus

Japanese flounder, By サフィル, CC BY-SA 4.0, Link.

A third flatfish genome was published near the end of this year. Here, among other things, the authors studied one of the most intriguing aspects of flatfish: their asymmetry. Flatfishes start out life as symmetrical larvae, but one eye migrates to other side during development. Thyroid hormone and retinoic acid were found to be important in signaling this development. Unexpectedly, visual pigments are also expressed in the skin to help orchestrate this asymmetrical body development!

Source. doi: 10.1038/ng.3732

Tiger tail seahorse, Hippocampus comes

Hippocampus erectus,
By Will Thomas, CC BY 2.0
Link 1. Link 2.
The seahorse is so unusual it is unclear to many that they are even fish. The authors of this study were interested in genes that underlie some of its unique traits. They found the seahorse genome has the highest evolutionary rate of any of the fish genomes they compared it with. Numerous duplicates of a particular gene (patristacin) were found that was expressed in the male brood pouch, which may be necessary for male pregnancy. A similar gene is also expanded in the live-bearing platyfish that shows female pregnancy, showing that, in this case, different genes in two different fish can play a similar role in pregnancy. In addition, tbx4 is absent from the seahorse genome. This gene is involved in regulating the development of hind limbs, which in fish are the pelvic fins. The absence of this gene is consistent with the absence of pelvic fins in seahorses. The authors of the study then knocked out this gene in zebrafish, and the zebrafish developed without pelvic fins, providing more evidence of its role in pelvic fin development. Finally, lack of certain genes involved with enamel development are missing from the seahorse genome, consistent with the lack of teeth in seahorses. 

Source. doi: 10.1038/nature20595

Gulf pipefish, Syngnathus scovelli

Syngnathus acus, By © Hans Hillewaert, CC BY-SA 4.0, Link.
The gulf pipefish and the seahorse are closely related, and coincidentally their genome sequences were published within a few days of each other. Like seahorses, gulf pipefish lack pelvic fins, teeth, and the males have a brood pouch. These shared adaptations arise from shared genomic characteristics. As with the seahorse genome, these authors found duplicates of the gene patristacin and confirmed they were expressed in the male pipefish brood pouch, and they also found the loss of tbx4 that could be implicated in hind limb loss. 

Source. doi: 10.1186/s13059-016-1126-6

Trinidadian guppy, Poecilia reticulata

Guppy, By Wibowo Djatmiko (Wie146) CC BY-SA 3.0, Link.
The guppy is an important species in studying evolution as an example of rapid adaptation and sexual selection. The genome sequence of the guppy will be informative for understanding the genetics of how this rapid adaptation occurs. By sequencing both male and female guppies, the authors of the study were able to identify genes that were specific to the Y chromosome involved in sex determination, as well as the difference in size and coloration of males compared to females.

Link. doi: 10.1371/journal.pone.0169087

66 other teleost genomes!

Atlantic cod, By Peter from Edinburgh, Scotland,
Uploaded by Amada44, CC BY 2.0. Link.
In the largest study of its kind, 66 partial teleost genomes were simultaneously published in a study looking at the evolution of cod-like fishes (order Gadiformes). The sequencing of the Atlantic cod genome (Gadus morhua) showed that cod lack some of their immune genes (MHC II genes). To compensate, cod have numerous copies of another class of immune genes (MHC I genes). By sequencing the genomes of many species across Gadiformes, the group to which cod belongs to, it turns out that the loss of MHC II is shared by all members of this order, and hence they inherited this loss from their common ancestor. The authors also found evidence that an increase in copies of MHC I genes is correlated with increased rates of speciation in these fishes, which is one of the first studies to my knowledge that finds support for a specific pattern of gene evolution as a cause for generating biodiversity in fishes. Although these genomes are not as high quality and are therefore not as complete as the other genomes that have been published this year, these sequences still provide more opportunity for genome comparisons between fish species, and provide the foundation for future, more-complete genome projects on these species.

Source. doi: 10.1038/ng.3645

With the increased ease of sequencing and assembling genomes, it has also become clear that genome sequences are not the end-all-be-all of biological understanding. By combining new genomes with comparisons of other genome sequences, studies of gene expression through development and in different regions of the body, and testing the function of genes by performing developmental biology experiments in other species, more insights can be gained into the origins of fish biodiversity. More fish genomes will continue to be sequenced, assembled, and mapped in 2017, providing even more opportunities to learn about fish for years to come!

* For people interested in minutiae, I am including species in this list that have been accepted for publication and made available online within 2016, rather than species with an official publication date within 2016. This means that Pimephales promelas and Seriola quinqueradiata, which had their genomes made available in 2015, but not officially published until 2016, were too early to make the cut.