Abstract
Gene duplication and subsequent divergence can lead to the evolution of new functions and lineage‐specific traits. In sticklebacks, the successive duplication of a mucin gene (MUC19) into a tandemly arrayed, multigene family has enabled the production of copious amounts of ‘spiggin’, a secreted adhesive protein essential for nest construction. Here, we examine divergence between spiggin genes among three‐spined sticklebacks (Gasterosteus aculeatus) from ancestral marine and derived freshwater populations, and propose underpinning gene duplication mechanisms. Sanger sequencing revealed substantial diversity among spiggin transcripts, including alternatively spliced variants and interchromosomal spiggin chimeric genes. Comparative analysis of the sequenced transcripts and all other spiggin genes in the public domain support the presence of three main spiggin lineages (spiggin A, spiggin B and spiggin C) with further subdivisions within spiggin B (B1, B2) and spiggin C (C1, C2). Spiggin A had diverged least from the ancestral MUC19, while the spiggin C duplicates had diversified most substantially. In silico translations of the spiggin gene open reading frames predicted that spiggins A and B are secreted as long mucin‐like polymers, while spiggins C1 and C2 are secreted as short monomers, with putative antimicrobial properties. We propose that diversification of duplicated spiggin genes has facilitated local adaptation of spiggin to a range of aquatic habitats.
Highlights
Gene duplication can lead to an increase in protein product and – following the divergence of duplicated genes – novel protein functions (Ohno 1970; Lynch & Force 2000) and lineage specific traits (Wu et al 2009; Vonk et al 2013)
From the three freshwater (Edinburgh) and three marine (Gullmarsfjord) G. aculeatus fish, 237 clones partially sequenced with M13 forward and reverse primers were identified as spiggin transcripts thorough BLASTN searches (E value < 1e-18)
From P. pungitius, a total of 127 partially sequenced clones showed significant sequence similarity (E value < 1e-18) to published spiggin sequences, including two interchromosomal chimeric transcripts identified through BLAT searches of the G. aculeatus draft assembly
Summary
Gene duplication can lead to an increase in protein product and – following the divergence of duplicated genes – novel protein functions (Ohno 1970; Lynch & Force 2000) and lineage specific traits (Wu et al 2009; Vonk et al 2013). In a study of recentlyduplicated genes in bacteria, archaea and eukaryotes, Kondrashov et al (2002) found that most of these genes were involved in environmental interactions, with a significant proportion encoding membrane or secreted proteins. Gene duplication has been suggested as a general mechanism promoting adaptation to novel environmental conditions (Kondrashov 2012). A multi-gene family (Jones et al 2001; Kawasaki et al 2003; Kawahara & Nishida 2006, 2007) is known to encode the protein component of a glue (‘spiggin’) that is produced in the kidney of males and used in the construction of nests (Wootton 1976; Jakobsson et al 1999). The ancestral spiggin gene is thought to have originated from the duplication of the single copy vertebrate mucin gene, MUC19, with duplication occurring both before and after the divergence of three-spined (Gasterosteus aculeatus) and nine-spined (Pungitius pungitius) sticklebacks
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