Functional similarity and molecular divergence of a novel reproductive transcriptome in two male-pregnant Syngnathus pipefish species
Article first published online: 20 SEP 2013
© 2013 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd.
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Ecology and Evolution
Volume 3, Issue 12, pages 4092–4108, October 2013
How to Cite
Ecology and Evolution 2013; 3(12): 4092–4108
- Issue published online: 23 OCT 2013
- Article first published online: 20 SEP 2013
- Manuscript Accepted: 12 AUG 2013
- Manuscript Revised: 6 AUG 2013
- Manuscript Received: 2 JUL 2013
- National Science Foundation
- American Museum of Natural History Lerner-Gray
- Sigma Xi
- Michigan State University
- Male pregnancy;
- molecular evolution;
Evolutionary studies have revealed that reproductive proteins in animals and plants often evolve more rapidly than the genome-wide average. The causes of this pattern, which may include relaxed purifying selection, sexual selection, sexual conflict, pathogen resistance, reinforcement, or gene duplication, remain elusive. Investigative expansions to additional taxa and reproductive tissues have the potential to shed new light on this unresolved problem. Here, we embark on such an expansion, in a comparison of the brood-pouch transcriptome between two male-pregnant species of the pipefish genus Syngnathus. Male brooding tissues in syngnathid fishes represent a novel, nonurogenital reproductive trait, heretofore mostly uncharacterized from a molecular perspective. We leveraged next-generation sequencing (Roche 454 pyrosequencing) to compare transcript abundance in the male brooding tissues of pregnant with nonpregnant samples from Gulf (S. scovelli) and dusky (S. floridae) pipefish. A core set of protein-coding genes, including multiple members of astacin metalloprotease and c-type lectin gene families, is consistent between species in both the direction and magnitude of expression bias. As predicted, coding DNA sequence analysis of these putative “male pregnancy proteins” suggests rapid evolution relative to nondifferentially expressed genes and reflects signatures of adaptation similar in magnitude to those reported from Drosophila male accessory gland proteins. Although the precise drivers of male pregnancy protein divergence remain unknown, we argue that the male pregnancy transcriptome in syngnathid fishes, a clade diverse with respect to brooding morphology and mating system, represents a unique and promising object of study for understanding the perplexing evolutionary nature of reproductive molecules.