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. 2016 Feb 1:16:30.
doi: 10.1186/s12862-016-0597-0.

Convergent evolution of hemoglobin switching in jawed and jawless vertebrates

Kim Rohlfing  1 , Friederike Stuhlmann  2 , Margaret F Docker  3 , Thorsten Burmester  4
Affiliations

Convergent evolution of hemoglobin switching in jawed and jawless vertebrates

Kim Rohlfing et al. BMC Evol Biol. .

Abstract

Background: During development, humans and other jawed vertebrates (Gnathostomata) express distinct hemoglobin genes, resulting in different hemoglobin tetramers. Embryonic and fetal hemoglobin have higher oxygen affinities than the adult hemoglobin, sustaining the oxygen demand of the developing organism. Little is known about the expression of hemoglobins during development of jawless vertebrates (Agnatha).

Results: We identified three hemoglobin switches in the life cycle of the sea lamprey. Three hemoglobin genes are specifically expressed in the embryo, four genes in the filter feeding larva (ammocoete), and nine genes correspond to the adult hemoglobin chains. During the development from the parasitic to the reproductive adult, the composition of hemoglobin changes again, with a massive increase of chain aHb1. A single hemoglobin chain is expressed constitutively in all stages. We further showed the differential expression of other globin genes: Myoglobin 1 is most highly expressed in the reproductive adult, myoglobin 2 expression peaks in the larva. Globin X1 is restricted to the embryo; globin X2 was only found in the reproductive adult. Cytoglobin is expressed at low levels throughout the life cycle.

Conclusion: Because the hemoglobins of jawed and jawless vertebrates evolved independently from a common globin ancestor, hemoglobin switching must also have evolved convergently in these taxa. Notably, the ontogeny of sea lamprey hemoglobins essentially recapitulates their phylogeny, with the embryonic hemoglobins emerging first, followed by the evolution of larval and adult hemoglobins.

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Figures

Fig. 1
Fig. 1
Expression profiles of sea lamprey aHbs quantified by RNA-seq. The aHb genes were displayed as predominantly expressed in the embryonic (a), larval (b), adult-parasitic (c) and adult-reproductive (d) stages. aHb7 (e) was not assigned to any specific developmental stage. The expression level is indicated as arbitrary units (AU), relative to the highest RPKM of the pool of adult-reproductive aHb1 expression, which is set to 100. Note that the expression levels of aHb2a and aHb2c, and aHb5a and aHb5b, respectively, were almost identical
Fig. 2
Fig. 2
Quantification of mRNA levels of selected sea lamprey globins. Adult blood (a) or whole ammocoete (b) were used. The transcript abundance was quantified by qRT-PCR of aHb1, aHb5a, aHb6, aHb7, aHb11, aHb12 (a, b)
Fig. 3
Fig. 3
Expression profiles of sea lamprey globins quantified by RNA-seq. The expression level of aMb1, aMb2, Cygb, GbX1 and GbX2 are indicated as AU (see above). The mRNA levels of aMb2, Cygb, GbX1, GbX2 were additionally displayed in the inset
Fig. 4
Fig. 4
Mapping of the stage specific expression patterns onto a Bayesian phylogenetic tree of sea lamprey globins. The developmental stages are shaded in different grey scales. The numbers at the nodes are posterior probabilities. The bar represents 0.3 PAM distance
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