Haemoglobin polymorphisms affect the oxygen-binding properties in Atlantic cod populations

Abstract

A major challenge in evolutionary biology is to identify the genes underlying adaptation. The oxygentransporting haemoglobins directly link external conditions with metabolic needs and therefore represent a unique system for studying environmental effects on molecular evolution. We have discovered two haemoglobin polymorphisms in Atlantic cod populations inhabiting varying temperature and oxygen regimes in the North Atlantic. Three-dimensional modelling of the tetrameric haemoglobin structure demonstrated that the two amino acid replacements Met55b 1 Val and Lys62b 1 Ala are located at crucial positions of the a 1 b 1 subunit interface and haem pocket, respectively. The replacements are proposed to affect the oxygen-binding properties by modifying the haemoglobin quaternary structure and electrostatic feature. Intriguingly, the same molecular mechanism for facilitating oxygen binding is found in avian species adapted to high altitudes, illustrating convergent evolution in water-and air-breathing vertebrates to reduction in environmental oxygen availability. Cod populations inhabiting the cold Arctic waters and the low-oxygen Baltic Sea seem well adapted to these conditions by possessing the high oxygen affinity Val55-Ala62 haplotype, while the temperature-insensitive Met55-Lys62 haplotype predominates in the southern populations. The distinct distributions of the functionally different haemoglobin variants indicate that the present biogeography of this ecologically and economically important species might be seriously affected by global warming.

The Future of Baltic Sea Populations: Local Extinction or Evolutionary Rescue?

“…The clines are explained either as a consequence of differential selection on individual gene loci, favoring one type of genes inside the Baltic Sea and another outside, or lack of gene exchange (migration) between Baltic and North Sea populations, or both. Evidence of selection for particular gene variants inside the Baltic Sea is particularly strong in blue mussels (Riginos and Cunningham 2005), Baltic clam (Luttikhuizen et al, unpublished data), herring (Larsson et al 2007;André et al 2010), and cod (Andersen et al 2009). …”

“…Baltic cod, for example, has a genetic variant of hemoglobin with two mutations that differ from hemoglobin of North Sea cod (Andersen et al 2009) (Fig. 4).…”

“…However, recent studies of genetic structure of species of marine fishes, invertebrates, algae, and plants have changed this paradigm and show numerous examples of structured species (reviewed in Hellberg 2009) in which populations are locally adapted (Hemmer-Hansen et al 2007;Larsen et al 2008;Andersen et al 2009;Larmuseau et al 2010). An important consequence of species being divided into locally adapted populations that may have key roles in their local ecosystem is that an extinct local population may not easily be replaced by recruits from other areas.…”

Repeated evolution of reproductive isolation in a marine snail: unveiling mechanisms of speciation

“…The latter can be identified, among other approaches, from associations between ecotype and single variable nucleotides (SNPs), by looking for genome regions with decreased diversity, probably produced by selective sweeps, or by comparing silent and non-silent substitution ratios in candidate genes. For a single candidate gene, it is also possible to relate sequence variation between alleles to differences in their functional properties (Andersen et al 2009). Using the microarray technique, we can compare expression levels of many genes in contrasting habitats or ecotypes, to estimate divergence at the transcriptomic level and at the same time identify more loci involved in ecotype differences (Ranz & Machado 2006;Shiu & Borevitz 2008).…”

Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management

“…Environmental variation and potential barriers to dispersal possibly affecting different species in similar manner include a temperature and salinity gradient (spanning 3-30 per mille; HELCOM 2010) reaching from the entrance of the Baltic Sea to the north of the Bothnian Bay (Gabrielsen et al 2002), and several sub-basins between which water circulation is partially restricted by submarine sills (HELCOM 2010). Species with both freshwater and marine origin have established populations which in many cases have undergone adaptations to the brackish water environment over the very short evolutionary history of the sea (Andersen et al 2009;Gaggiotti et al 2009;Papakostas et al 2012).…”