Insights into body size variation in cetaceans from the evolution of body-size-related genes

Yingying Sun,Shixia Xu,Xiaohui Sun,Yurui Lin,Daiqing Yin,Yanzhi Liu,Guang Yang

doi:10.1186/s12862-019-1461-9

Abstract

BackgroundCetaceans exhibit an exceptionally wide range of body size, yet in this regard, their genetic basis remains poorly explored. In this study, 20 body-size-related genes for which duplication, mutation, or deficiency can cause body size change in mammals were chosen to preliminarily investigate the evolutionary mechanisms underlying the dramatic body size variation in cetaceans.ResultsWe successfully sequenced 20 body-size-related genes in six representative species of cetaceans. A total of 46 codons from 10 genes were detected and determined to be under strong positive selection, 32 (69.6%) of which were further found to be under radical physiochemical changes; moreover, some of these sites were localized in or near important functional regions. Interestingly, positively selected genes were well matched with body size evolution: for small cetaceans, strong evidence of positive selection was detected at ACAN, OBSL1, and GRB10, within which mutations or duplications could cause short stature; positive selection was found in large cetaceans at CBS and EIF2AK3, which could promote growth, and at the PLOD1 gene, within which mutations could cause tall stature. Importantly, relationship analyses revealed that the evolutionary rate of CBS was positively related to body length and body mass with statistical significance. Additionally, we identified 32 cetacean-specific amino acid changes in 10 genes.ConclusionsThis is the first study to investigate the molecular basis of dramatic body size variation in cetaceans. Our results provide evidence of the positive selection of several body-size-related genes in cetaceans, as well as divergent selection between large or small cetaceans, which suggest cetacean body size variation possibly associated with these genes. In addition, cetacean-specific amino acid changes might have played key roles in body size evolution after the divergence of cetaceans from their terrestrial relatives. Overall, the evolutionary pattern of these body-size-related genes could provide new insights into genetic mechanisms for the body size variation in cetaceans.

Highlights

Cetaceans exhibit an exceptionally wide range of body size, yet in this regard, their genetic basis remains poorly explored
The one-ratio model, which assumes that one ratio occurs across the phylogenetic tree, showed that the ω ratios of 20 body-size-related genes ranged from 0.009 to 0.332, which indicates that strong purifying selection acts on these genes to constrain their important functions in body size development
The likelihood ratio test (LRT) showed that M8 fitted the data better than M8a at 10 genes (i.e., ACAN, aryl hydrocarbon receptor interacting protein (AIP), cyclindependent kinase inhibitor 1B (CDKN1B), translation initiation factor2-α kinase 3 (EIF2AK3), FBN1, mediator complex subunit 12 (MED12), MEN1, Natriuretic peptide receptor 2 (NPR2), nuclear receptor binding SET domain protein 1 (NSD1), and obscurin-like 1 (OBSL1)), with 65 codons identified to be under positive selection using the Bayes Empirical Bayes (BEB) approach with posterior probabilities ≥0.85 (Table 1)

Summary

Introduction

Cetaceans exhibit an exceptionally wide range of body size, yet in this regard, their genetic basis remains poorly explored. The evolutionary rate of body mass in cetaceans exceeds that of terrestrial mammals perhaps due to “aquatic weightlessness”, migratory behaviour, and selection related to thermoregulation and feeding ecology in an aquatic environment [14]. Among these factors, temperature was reported to affect the body size of cetaceans, in agreement with Bergmann’s rule that animals living in colder climates are generally larger than those living in warmer regions [15]. Dolphins and porpoises, generally much smaller than whales, e.g., vaquita Phocoena sinus, the smallest cetacean, is only 1.4 m in body length and 42 kg in body mass and usually lives close to shore in shallow water. The genetic bases of dramatic body size variation in cetaceans remain poorly explored

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Conclusion