Genome Evolution in Amphibians

Abstract

Genome size variation in vertebrates reflects an amazing amount of genetic and genomic diversity. C‐value (genome size) ranges from 0.4 picograms (pg) in pufferfish to 133 pg in the marbled lungfish. Most vertebrate lineages have characteristic average C‐values with restricted ranges. Amphibia, in contrast, represent an extreme: C‐values in salamanders range from around 13 to over 122 pg; in frogs, they range from under 1 to over 13 pg. Why would closely related lineages and species have such dramatic differences in C‐value? A number of theories have been proposed to account for the extreme range in genome size found in all eukaryote taxa. The amphibia not only have a wide range of C‐values, but they also have a correspondingly wide range of life history traits and other phenotypes such as neoteny and limb regeneration. This remarkable class of vertebrate thus provides a unique model system for addressing evolutionary and physiological hypotheses.

Key Concepts

  • Junk DNA (retroviruses and DNA transposons) infected the ancestral eukaryote cell and established, together with mitochondria, a symbiotic relationship from which all other eukaryotic life forms emerged.
  • The host response to the original infection was adaptive rather than purifyingly selective: junk DNA provided the conditions for the emergence of a checkpoint guardian of the genome and correspondingly enhanced genome stability.
  • As genome size expanded, DNA repair systems increased in efficiency, allowing for the acquisition of new genes and new adaptations.
  • DNA replication programs and gene transcription programs reorganised as genome size either increased or decreased over evolutionary time.
  • Species richness negatively correlates with genome stability and positively correlates with karyotype diversity within specific lineages.
  • DNA damage response and repair (DDR) programs have evolved differentially in r and K‐strategists: large body organisms have enhanced DDRs compared to small body, short‐lived organisms, and hence they tend to have more deterministic and organised replication programs.
  • Junk DNA serves as a substrate for the DDR to protect the cell against ‘mitotic catastrophe’.
  • Junk DNA serves as a scaffold for the formation of facultative heterochromatin during development and speciation,and hence participates in the global tissue‐specific and species‐dependent transcription programs.

Keywords: genome stability; amphibia; genome size; karyotype diversity; species richness; heterochromatin; cell cycle checkpoint; DNA damage response; junk DNA; transposons

Figure 1. Box plots comparing genome size variation in Urodela, PACS (Proteidae, Amphiumidae, Cryptobranchidae, Sirenidae), Anura, Gymnophiona and Mammalia. The species average genome size was determined from the data available in the Animal Genome Size Database. C‐values in Urodela (n = 219) span a range of over 120 pg, with a median of approximately 30 pg skewed right towards larger C‐values. PACS (n = 14) are all obligate paedomorphs. C‐value in this group spans a range of 20 to 120 pg, with a median size of 55 pg. Frog (n = 285) C‐values span a range of less than 1 pg to over 13 pg, narrowly distributed about a median of approximately 4.5 pg. Gymnophiona (n = 3) exhibit a wider, more highly skewed distribution compared to frogs. Mammals (n = 593), with a narrower distribution of C‐values spanning approximately 2–9 pg, are included for comparison (median: approximately 3 pg).
Figure 2. Phylogenetic tree of Urodela families. Divergence times are indicated in millions of years at the top and bottom of the figure. C‐value, body size and species richness are shown on the y‐axis. The key shows the colour coding for each variable. Scale for species richness is indicated by the size of the grey circles. Among sister pairs (Cryptobranchidae:Hynobidae; Ambystomatidae:Dicampodontidae; Amphiumidae:Plethodontidae), a clear pattern emerges: C‐value and species richness are inversely related. This pattern is independent of body size and apparent across the different salamander lineages. Herrick and Sclavi (). Reproduced with permission of Elsevier.
Figure 3. Evolution of salamander genome size. Time of origin (Timetree.com) is represented in Million Years Ago (Mya) on the x‐axis; average C‐value for each genus is represented on the y‐axis. The key indicates the name of each genus plotted on the graph. The positive slope (approximately 1 pg/Mya) indicates that older lineages tend to have larger genomes, suggesting either an increase in C‐value with time or, conversely, an overall decrease as new taxa emerge and radiate. Molecular diversity, in terms of genome size and mutation rate variations, tends to be associated with smaller genomes and comparatively more recent adaptive radiations (less than ancestral C‐value = 43 pg). Older genera with larger genomes tend to be comparatively more genetically stable (greater than or equal to ancestral C‐value). Herrick and Sclavi (). Reproduced with permission of Elsevier.
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Herrick, John, and Sclavi, Bianca(May 2020) Genome Evolution in Amphibians. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028996]