Convergent evolution of antifreeze glycoproteins in Antarctic notothenioid fish and Arctic cod

Abstract

Antarctic notothenioid fishes and several northern cods are phylogenetically distant (in different orders and superorders), yet produce near-identical antifreeze glycoproteins (AFGPs) to survive in their respective freezing environments. AFGPs in both fishes are made as a family of discretely sized polymers composed of a simple glycotripeptide monomeric repeat. Characterizations of the AFGP genes from notothenioids and the Arctic cod show that their AFGPs are both encoded by a family of polyprotein genes, with each gene encoding multiple AFGP molecules linked in tandem by small cleavable spacers. Despite these apparent similarities, detailed analyses of the AFGP gene sequences and substructures provide strong evidence that AFGPs in these two polar fishes in fact evolved independently. First, although Antarctic notothenioid AFGP genes have been shown to originate from a pancreatic trypsinogen, Arctic cod AFGP genes share no sequence identity with the trypsinogen gene, indicating trypsinogen is not the progenitor. Second, the AFGP genes of the two fish have different intron-exon organizations and different spacer sequences and, thus, different processing of the polyprotein precursors, consistent with separate genomic origins. Third, the repetitive AFGP tripeptide (Thr-Ala͞Pro-Ala) coding sequences are drastically different in the two groups of genes, suggesting that they arose from duplications of two distinct, short ancestral sequences with a different permutation of three codons for the same tripeptide. The molecular evidence for separate ancestry is supported by morphological, paleontological, and paleoclimatic evidence, which collectively indicate that these two polar fishes evolved their respective AFGPs separately and thus arrived at the same AFGPs through convergent evolution.

Genotype networks shed light on evolutionary constraints

“…Not surprisingly, important phenotypic adaptations are directly traceable to changes in macromolecules. Examples include antifreeze proteins that can enable an organism to survive at low temperatures, and globin molecules adapted to oxygen transport at extremely high altitudes exceeding 10 kilometers [37][38][39][40].…”

“…Not surprisingly, important phenotypic adaptations are directly traceable to changes in macromolecules. Examples include antifreeze proteins that can enable an organism to survive at low temperatures, and globin molecules adapted to oxygen transport at extremely high altitudes exceeding 10 kilometers [37][38][39][40].In all three system classes, it has recently become possible to gain a better understanding of the relationship between genotype and phenotype. One reason is that sufficiently large amounts of empirical data exist to analyze this relationship, as in the case of proteins.…”

How insects survive the cold: molecular mechanisms—a review

“…Comparison of sequence data from these four insects reveals very little sequence similarity between them, indicating that similar to the situation of antifreeze evolution in teleost fish (Chen et al, 1997), insect AFPs have evolved independently from different progenitors (Graham and Davies, 2005). Again, similarly to fish, the AFPs studied in detail consist of multi-gene families with at least 17 isoforms of cfAFP (Doucet et al 2002;Tyshenko et al 2005) and 13 isoforms of DAFP (Andorfer and Duman, 2000) Cold insect review characterised to date.…”

Flies expand the repertoire of protein structures that bind ice

“…An example of this environmental bonanza is illustrated by the sudden proliferation and radiation of notothenioid fishes into the ice-laden Antarctic Ocean during the Cenozoic ice ages (1) after they acquired antifreeze glycoproteins (2). Antifreeze proteins (AFPs) bind to ice and prevent seed ice crystals from growing and damaging the host organism (3).…”