Gene cooption without duplication during the evolution of a male-pregnancy gene in pipefish

Abstract

Comparative studies of developmental processes suggest that novel traits usually evolve through the cooption of preexisting genes and proteins, mainly via gene duplication and functional specialization of paralogs. However, an alternative hypothesis is that novel protein function can evolve without gene duplication, through changes in the spatiotemporal patterns of gene expression (e.g., via cis-regulatory elements), or functional modifications (e.g., addition of functional domains) of the proteins they encode, or both. Here we present an astacin metalloprotease, dubbed patristacin, which has been coopted without duplication, via alteration in the expression of a preexisting gene from the kidney and liver of bony fishes, for a novel role in the brood pouch of pregnant male pipefish. We examined the molecular evolution of patristacin and found conservation of astacin-specific motifs but also several positively selected amino acids that may represent functional modifications for male pregnancy. Overall, our results pinpoint a clear case in which gene cooption occurred without gene duplication during the genesis of an evolutionarily significant novel structure, the male brood pouch. These findings contribute to a growing understanding of morphological innovation, a critically important but poorly understood process in evolutionary biology.novel trait evolution ͉ patristacin ͉ Syngnathidae E volutionary innovation has been defined as ''the origin of a novel body part which may serve a novel function or specialize in a function that was already performed in the ancestral lineage but without a dedicated organ' ' (ref. 1, p. 581). In seahorses and pipefishes (family Syngnathidae) males carry their embryos on their ventral surface, either exposed to the environment or enclosed in a fleshy brood pouch (Fig. 1). The brood pouch is a clear example of an evolutionary innovation: syngnathids are the only lineage to have evolved a morphological structure that allows males to become pregnant. In many species of syngnathid fishes, the brood pouch is a complex organ composed of highly vascularized epithelial tissue that forms a honeycomb matrix encapsulating individual eggs during gestation ( Fig. 1) (2). This placenta-like tissue apparently supplies nutrients to developing embryos (3) in a manner analogous to the placenta of female mammals. The pouch is lined with cells rich in mitochondria (CRMs) (Fig. 1) (2, 4) that transfer ions between the brood pouch fluid and the male bloodstream, maintaining an osmotically neutral environment during the early stages of gestation (4-6). A phylogeny of the Syngnathidae suggests two independent origins of the brood pouch based on its location on either the abdomen (Gastrophori) or the tail (Urophori) of the male (7), and within these two lineages there is considerable variation in the degree to which the pouch encloses developing embryos, the complexity of the ''pseudoplacenta,'' and the structure of brood pouch folds (7).Clearly, the evolution of a structure as complex as a brood pouch req...

Lysine Decarboxylase Catalyzes the First Step of Quinolizidine Alkaloid Biosynthesis and Coevolved with Alkaloid Production in Leguminosae

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Adaptive evolution of the uncoupling protein 1 gene contributed to the acquisition of novel nonshivering thermogenesis in ancestral eutherian mammals

“…On the other hand, an example of acquisition of novel gene function without gene duplication has been reported (Piatigorsky and Wistow, 1991;Messier and Stewart, 1997;Harlin-Cognato et al, 2006). However, whether or not this mode of evolutionary innovation is a prevalent case is unclear, since it seems difficult to acquire novel gene function without redundant duplicated gene.…”

The genome of the Gulf pipefish enables understanding of evolutionary innovations

“…To this end, we produced an annotated chromosome-level genome model [5] for S. scovelli by integrating a 176X-coverage, short-read genome assembly with a linkage map constructed from RAD-seq markers. We used this tool to reveal features of chromosome structure evolution, to investigate pipefish lineage-specific losses of genes associated with morphological development, to infer the likely phylogenetic position of the syngnathids in the tree of ray-finned fishes, and to describe a unique cluster of tandemly duplicated patristacins [18] that demonstrate conspicuous expression changes in the brood pouch during male pregnancy. Others have reviewed the approaches best suited to small-scale genome projects [19], but our intention here is to provide a biological case study and methodological template for success, motivated by the desire to better understand how novelties arise.…”