Longer or shorter spines: Reciprocal trait evolution in stickleback via triallelic regulatory changes inStanniocalcin2a

Abstract

Vertebrates have repeatedly modified skeletal structures to adapt to their environments. The threespine stickleback is an excellent system for studying skeletal modifications, as different wild populations have either increased or decreased the lengths of their prominent dorsal and pelvic spines in different freshwater environments. Here we identify a regulatory locus that has a major morphological effect on the length of stickleback dorsal and pelvic spines, which we term Maser (major spine enhancer). Maser maps in a closely linked supergene complex that controls multiple armor, feeding, and behavioral traits on chromosome IV. Natural alleles in Maser are differentiated between marine and freshwater sticklebacks; however, alleles found among freshwater populations are also differentiated, with distinct alleles found in short- and long-spined freshwater populations. The distinct freshwater alleles either increase or decrease expression of the bone growth inhibitor gene Stanniocalcin2a in developing spines, providing a simple genetic mechanism for either increasing or decreasing spine lengths in natural populations. Genomic surveys suggest many recurrently differentiated loci in sticklebacks are similarly specialized into three or more distinct alleles, providing multiple ancient standing variants in particular genes that may contribute to a range of phenotypes in different environments.

Evolution of static allometry and constraint on evolutionary allometry in a fossil stickleback

“…Accordingly, weaker allometry of armour traits would be favourable in freshwater. Indeed, armour phenotypes of extant Threespine Stickleback tend to be polygenic, and the genes for them tend to be unlinked (Colosimo et al, 2004 ; Cresko et al, 2004 ; Howes et al, 2017 ; Indjeian et al, 2016 ; Roberts Kingman et al, 2021 ; Roberts Kingman et al, 2021 ; Shapiro et al, 2004 ). This genetic architecture could spread geographically during gene flow between marine and freshwater fish (the transporter hypothesis; Jones et al, 2012 ; Roberts Kingman et al, 2021 ; Schluter & Conte, 2009 ) and become a general characteristic of the species.…”

Evolution of stickleback spines through independentcis-regulatory changes atHOXDB

“…The QTL peak on the distal end of chromosome 6 includes the HOXDB cluster drawn below the plot. The major peak for DS2 length on chromosome 4 contains the EDA-MSX2A-STC2A supergene complex, which has been described elsewhere (Howes et al, 2017;Roberts Kingman et al, 2021a). Dashed lines: genome-wide significance threshold based on permutation testing.…”

“…Many of the recently evolved populations show loss or reduction of structures previously present in ancestral forms, including loss of armor plates, loss of the pelvic hind fins, reduction of spine lengths, and reduction of body pigmentation (Chan et al, 2010;Colosimo et al, 2005;Howes et al, 2017;Miller et al, 2007). However, recently derived populations can also evolve increases in size or number of structures, including increased body size, increased number of teeth, increased spine length, and increased number of spines in the dorsal midline (Cleves et al, 2014;Moodie, 1972;Roberts Kingman et al, 2021a;Spoljaric and Reimchen, 2011). Here, we use genetic and genomic approaches in two different stickleback genera to study the molecular mechanisms involved in spine patterning changes in natural populations.…”

“…The number, length, and morphology of bony spines differ substantially among species, and the spines can be freestanding or incorporated into segmented rays within the dorsal and anal fins (Mabee et al, 2002). Recent studies have begun to reveal how spines form and grow within the median fin fold of developing fish (Höch et al, 2021; Howes et al, 2017; Roberts Kingman et al, 2021a). However, little is known about the detailed molecular changes that underlie the diverse patterns of spines seen in different fish species.…”

Evolution of stickleback spines through independent cis-regulatory changes at HOXDB

“…The number, length and morphology of bony spines differ substantially among species 25 . Recent studies have begun to reveal how spines form and grow within the median fin fold of developing fish [26][27][28] . However, little is known about the molecular changes that underlie the diverse spine patterns seen in different species.…”