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This New Genome Shows How All Land Vertebrates Evolved, Including Ourselves

 

For decades, biologists have questioned how gill-bearing, finned fish evolved into air-breathing, limbed amphibians.

This debate focuses on representatives of a once much larger class of fish, which exhibit traits integral for such progression. Known as lobe-finned fish, this group is now largely extinct, apart from six lungfish species and two varieties of coelacanth. Quite dissimilar in biology, these two fish types have divided biologists who question which is more closely related to amphibians. To provide insight on these uncertainties, the coelacanth genome has been decoded. Published in the journal Nature, this study reinforces our understanding of how amphibians evolved, indicating whether lungfish or coelacanths are more closely related to limbed vertebrates, and indeed our own biological lineage.

It is often stated that during the Devonian period (360 to 420 million years ago) a primitive fish-like creature hauled itself out of its aquatic domain and onto dry land, commencing the amphibian realm. Of course, such a scenario is ridiculous. The processes that enable a group of organisms to leave a life in water and survive on land are extremely complex, occurred over geological time, and involved the environment selecting characteristics that are favourable to such organisms: the genes that express these traits gradually accumulate in subsequent generations.

Contrasting Lifestyles

There are four classes of fish with living representatives: jawless fish (lampreys and hagfish); cartilaginous fish (sharks and rays); ray-finned fish (eels, cod, salmon, pike, tuna and flatfish); and lobe-finned fish (coelacanths and lungfish). With large eyes for feeding on deep water animals, coelacanths have bony skeletons and fleshy, lobed-fins, joined to the body by scaly, stalk-like extensions, each containing a single bone. There are two living coelacanth species: inhabiting waters around East Africa and Madagascar, the West Indian Ocean coelacanth is the largest, growing to 2 metres; the other species was caught around Indonesia. Supporting paired lobe-fins, lungfish are otherwise quite different from coelacanths. Feeding on aquatic plants and animals, these fish have elongated bodies, inhabit freshwater systems in South America, Africa, and Australia, and have the ability to breathe air.  

With a fossil record ending in the Cretaceous period, 70 million years ago, 19th century palaeontologists assumed coelacanths went extinct with the dinosaurs. These views changed in 1938 when fishermen brought ashore a large, archaic-looking fish, caught off South Africa. This finding surprised Marjorie Courtenay-Latimer, the curator of a local museum, who sent a drawing of the specimen to Professor JLB Smith, an authority on fish. Smith identified the fish as a coelacanth: an event often described as the great zoological discovery of the 20th century (the species was called Latimeria chalumnae, in honor of Courtenay-Latimer). With lobe-fins, some scientists suspect coelacanths are the most closely related living animal to the ancestral amphibians; while other biologists consider lungfish to have an even closer relationship.

Some fish possess swim bladders — simple sacs that regulate buoyancy and enable gas exchange. It is from swim bladders that lungs developed; in higher vertebrate embryos, lungs form from vesicles that emerge from the oesophagus, in a similar manner to how swim bladders develop in fish. Lungs are more complex than swim bladders and are subdivided into smaller air-sacs, increasing internal surface areas for gas exchange. As well as gills, lungfish possess two lungs (except the Australian species, which has one) that are connected to the gullet. Only the Australian lungfish can sufficiently respire through its gills; in other species, gas exchange occurs predominantly via the lungs, which are inflated by gulping air through the mouth.

The lobed-pectoral fin of the marbled lungfish, which inhabits the River Nile and lake systems in tropical Africa, can be clearly seen

Despite belonging to the same biological class, the lifestyles of lungfish and coelacanths are quite different, and some biologists have expressed uncertainties over which is more closely related to land vertebrates. New genetic research, however, provides fascinating insight into such relationships.

Lungs or Limbs?

Modern coelacanths resemble their fossilized predecessors, found in rocks 300 million years old, indicating negligible changes in the animal's anatomy – and therefore genes – over geological time. To gain further understanding, researchers from the University of Uppsala in Sweden and the Broad Institute in the United States sequenced the coelacanth genome, which consisted of almost three billion base pairs. The research reveals that although there are some changes, the protein-coding genes, responsible for embryonic development, are significantly constant. Considering the coelacanth’s extreme and relatively stable environment, the lack of genetic changes are not too surprising. It is likely the fish adapted to living in the ocean depths, where there are few competitors, millions of years ago. When well suited to an ecological niche, there is no need to adapt further if the environment remains steady.

This research has been used to appreciate the relationships between coelacanths, lungfish and land vertebrates. Comparisons were made between the DNA profiles of coelacanths, lungfish and terrestrial vertebrates, including lizards, birds and mammals. Two hundred-fifty one genes that are similar in these different genomes were selected to appreciate evolutionary associations. From the results, it was apparent lungfish are more closely related to amphibians than coelacanths. The coelacanth genome also provided information about which genes were lost when vertebrates moved onto land, as well as what regulatory elements (which oversee where and when genes are activated) changed. This included regulatory changes that influence genes involved in smell perception, immunity, the ability to convert toxic ammonia into urea, and limb development.

The researchers also located a genetic sequence from the coelacanth’s genome that is found in land vertebrates but not in cartilaginous or ray-finned fish. When brought to the ocean’s surface, coelacanths die due to pressure changes and cannot be studied in aquariums. Accordingly, scientists inserted the DNA fragment into a mouse embryo and observed the outcome. This gene was responsible for forming bone in the wrists, fingers, ankles and toes of the developing mouse. Although it is not known what the function of this DNA sequence is within the coelacanth’s embryo, it has been suggested the gene was necessary for the development of appendages.

The fish-like form of a tadpole – the juvenile phase of a salamander, frog or toad’s life-cycle – is a vestige of the gill-bearing heritage of these animals

Changing Lifestyles

This research brings attention to an area of palaeontology steeped in mystery: how aquatic animals adapted to terrestrial lifestyles and what caused this phenomenon to occur. Amphibians were not the first organisms to move onto land: the predecessors of mosses and ferns had already colonized some terrestrial areas, as well as several invertebrates, including scorpions and millipedes. These early land ecosystems may to have lured the ancestral amphibians onto land to take advantage of new food sources. Sheltered swamp areas could also provide relatively safe environments for eggs and young, benefiting limb-like fins that can clamber through regions clogged with vegetation. Decaying plant matter in swamps may have lowered oxygen levels; thus, air-breathing fish would have had an advantage. The avoidance of predators is another theory: in Devonian rocks there are fossils of freshwater sharks, giant water scorpions and other large predatory animals that could have consumed the ancestral amphibians. The reality of such a progression, however, remains unknown.

Modern lungfish and coelacanths are not ancestral amphibians; such organisms adapted gradually over many generations and went extinct millions of years ago. Yet there is mounting evidence, supported by the coelacanth genome study, to indicate the predecessors of lungfish, which are distant relations of coelacanths, diverged in the  Devonian period and gave rise to organisms that led to the amphibians, and thus the reptiles, birds, mammals, and ourselves.  

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