The molecular evolution of spiggin nesting glue in sticklebacks

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.

Immigrant reproductive dysfunction facilitates ecological speciation

“…For example, salinity has a significant impact on parasites and pathogens, such as bacteria (Herlemann et al 2011) and oomycetes (Lehtonen and Kvarnemo 2015), and the prevalence of parasites and their intermediate hosts changes drastically over salinity gradients (Zander 2005;Rogowski and Stock-well 2006). In three-spined sticklebacks (Gasterosteus aculeatus), the molecular divergence between marine and freshwater forms of the nesting glue protein spiggin has been argued to be driven by selection on functional properties including antimicrobial effects (Seear et al 2015). In all these systems where we expect IRD to occur, multiple -and very different -traits are expected to be under divergent selection.…”

“…For example, selection on both osmoregulation and reproductive ability has been invoked to explain the divergence of Baltic Sea populations from Atlantic populations of Atlantic cod (Gadus morhua) (Berg et al 2015), and European flounder (Platichthys flesus) (Momigliano et al 2017), and this may also be true for other species that have diverged between the two environments (Serrao et al 1999;Johannesson and André 2006;Hemmer-Hansen et al 2007;Larmuseau et al 2009a;Johannesson et al, 2011;Limborg et al, 2012). In three-spined sticklebacks (Gasterosteus aculeatus), the molecular divergence between marine and freshwater forms of the nesting glue protein spiggin has been argued to be driven by selection on functional properties including antimicrobial effects (Seear et al 2015). For example, salinity has a significant impact on parasites and pathogens, such as bacteria (Herlemann et al 2011) and oomycetes (Lehtonen and Kvarnemo 2015), and the prevalence of parasites and their intermediate hosts changes drastically over salinity gradients (Zander 2005;Rogowski and Stock-well 2006).…”

The impact of selection, gene flow and demographic history on heterogeneous genomic divergence: three‐spine sticklebacks in divergent environments

“…It is striking that some of these regions contain QTLs for morphological traits, including lateral plates (Liu et al 2014;Miller et al 2014). Also, one region overlaps with the position of multiple copies of Spg1 (Chromosome 4, 21,002,172-21,221,912 bp), a multigene family coding for 'spiggin' nesting glue and assumed to be under selection reflecting local physicochemical conditions, such as salinity and pH (Seear et al 2015). Two of the regions were found to be consistent freshwater-marine outliers in the study by Hohenlohe et al (2010).…”

Architecture of parallel adaptation to freshwater in multiple populations of threespine stickleback

“…Genes that are likely to be involved in the differential adaptation to the two environments include osmoregulatory genes ATPase 1 alpha-subunit ATP1A1 and V-type ATPase VMA21 (DeFaveri et al 2011;Jones et al 2012), genes that encode important components of the immune system such as GARP (Colosimo et al 2005;Robertson et al 2017), and genes responsible for the embryogenesis WNT7B (Jones et al 2012) and development of the lateral plates and gill rakers, EDA and EDAR (Colosimo et al 2005;Jones et al 2012;Glazer et al 2014). A number of genes, such as MUC-like genes (Jones et al 2012;Seear et al 2015), may play a role in the pre-zygotic isolation between freshwater and marine individuals.…”