An ancient transpecific polymorphism shows extreme divergence in a multitrait cline in an intertidal snail (Nucella lapillus (L.))

Clines in intraspecific genetic variation are frequently associated with an environmental transition. Here,divergence among nucleotide sequences of tw o nuclear loci, cytosolic and mitochondrial malate dehydrogenase (cMDH and mMDH, respectively), is described, in a multitrait dine over a distance of ca. 3 km where shell phenotype, allozyme, mitochondrial DNA haplotype, and centric fusion (Robertsonian translocations) frequencies covary with temper ature and humidity and change abruptly in a continuous population of the do g-whelk (Nucella lapillus), a common intertidal snail of the north temperat e Atlantic. Protein electrophoresis has already shown two alleles of mMDH v arying from fixation of one allele to near fixation of the other, whereas c MDH appears to be monomorphic. The results of this study show a striking di sparity in nucleotide sequence divergence among alleles at the two loci, wi th extreme molecular differentiation in one of them. Four alleles of cMDH w ere found to have nucleotide and amino acid sequence divergences of 0.4% an d 0.3%, respectively. In contrast, the two mMDH cDNA alleles differed by 23 % and 20% at the nucleotide and amino acid levels, respectively. Analysis o f a 91-bp partial nucleotide sequence of nuMDH from Nucella freycineti, the closest relative of N. lapillus, revealed two similar alleles and indicate d that the divergence in mMDH in N. lapillus represents an ancient transpec ific polymorphism in these Nucella. Together with earlier studies on variat ion in N. lapillus, it is argued that the polymorphism in mMDH and the dine s in N. lapillus represent the presence of two persistent coadapted gene co mplexes, multitrait coevolving genetic solutions to environmental variation , which may presently enable this snail to exploit a diverse environment su ccessfully.