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To identify sequence convergence between marine mammal lineages, we employed a maximum likelihood ML approach 4 , 25 , hereafter termed likelihood convergence analysis. The likelihood convergence analysis revealed genes 7. Having identified putative convergent genes in marine mammals by evolutionary model analysis, we assessed the prevalence of parallel substitutions in the mammal dataset. As revealed by the aforementioned results for 62 mammals, the majority of parallel substitutions were not unique to each combination of two or three marine mammals Supplementary Fig.

Similarity, only 14 rapidly evolved genes 1. A Percentage of genes with parallel substitutions in rapidly evolving genes R , likelihood convergence genes L and 70 aquatic adaptation genes A. Red region denotes the proportion of parallel substitutions in marine mammals. C Percentage of genes with unique amino acid changes in rapidly evolving genes R , likelihood convergence genes L and 70 aquatic adaptation genes A.

Unique amino acid changes were classified into those changing in all three lineages of marine mammals III , in any two of the three marine lineages II and in single lineages of marine mammals I. In each plot, there are loci showing negative relationship, characterized by slopes significantly below zero, and loci showing positive relationship, with slopes greater than zero.

E Percentage of positively selected genes in rapidly evolving genes R , likelihood convergence genes L and 70 aquatic adaptation genes A. Positively selected genes were identified in cetaceans, pinnipeds, and sirenians, respectively. F Enriched network of 70 aquatic adaptation genes.

Evolutionary Biology, Overview (marine mammals)

Candidate genes are indicated by grey filled squares, missing genes by white filled triangles, and metabolites by white filled circles. Gene ontology categories are represented by Synaptic transmission in red, DNA replication in green, and Muscle contraction in blue. We next searched for unique amino acid residue changes in all three marine groups, any two marine groups and single marine groups.

Strikingly, most of the genes A similar trend was observed for the 70 candidate aquatic adaptation genes Fig. These data show that candidate genes for convergent evolution of aquatic mammals are primarily characterized by distinct amino acid changes in each marine group. Previous studies suggested that sequence convergence is a consequence of natural selection 4.

Of the rapidly evolving genes in marine mammals, only 13 genes 1. We further considered individual marine lineages. Positively selected genes PSGs in single marine lineage, i. Rapidly evolving genes contained a total of PSGs These data suggest that candidate aquatic adaptation genes rapidly evolving genes or likelihood convergence genes are co-influenced by lineage-specific selection with amino acid changes at distinct sites, a phenomenon previously observed for sodium channels associated with convergent evolution of electric organs in fish The specific roles of the candidate genes associated with aquatic adaptation require future functional analyses.

However, insights can be gained by functional gene ontology GO enrichment analysis.

In agreement, pathway analyses revealed a cellular network comprising 20 genes, including 10 of our candidate genes, centered on synaptic transmission and muscle contraction Fig. Nerve activity is a major control mechanism of the muscle fiber type profile, and multiple signaling pathways have been implicated in activity-dependent changes of muscle fibers For example, MYL1 encodes fast skeletal muscle myosin alkali light chains Altered expression of genes associated with the Wnt pathway has been implicated in metabolic and structural transformation of Weddel seal skeletal muscle from a strictly terrestrial lifestyle as a pup to an aquatic lifestyle adapted for deep dives as adult animals In response to hypoxic challenge a series of cellular responses are initiated in mammalian cells, triggering adaptive processes including changes in cell division, survival, motility, or differentiation Hypoxia markedly decreases total de novo transcription and, accordingly, several RNA-binding proteins RBPs have been found to affect the stability of many specific mRNAs.

The mRNA—protein complexes transition into stress granules, highly specialized cytoplasmic structures and sites of mRNA storage that facilitate translational reprogramming A recent study demonstrated a role for YBX1 in stress granule formation and tumor progression Taken together, the candidate aquatic adaptation genes encompass a plausible range of functional categories associated with marine lifestyles.

Our whole genome analyses revealed that parallel substitutions are widespread in marine mammals, consistent with a recent study by Foote and colleagues However, the majority of parallel substitutions are not unique to marine mammals. These findings do not rule out that parallel substitutions contribute to functional and phenotypic convergence of marine mammals. As the number of taxa increases, the likelihood of finding another homoplasious substitution in a terrestrial taxon increases as well.

Two lines of evidence from experimental studies support this hypothesis. For example, the transfer of three related bacteriophage species to a novel environment revealed a high rate of parallel genetic evolution at orthologous nucleotide and amino acid residues within, but not between, species Similarly, a study involving Pseudomonas aeruginosa demonstrated that antibiotic resistance and pathogen fitness in individual isolates stemmed from parallel substitutions in four antibiotic resistance genes coupled with distinct substitutions in more than hundred other genes 41 , Following submission of our manuscript, two studies were published arguing that there is no excess of parallel convergence between echolocating mammals 43 , They demonstrated that methods solely based on sitewise likelihood convergence are not adequate for measuring genomic convergence This is consistent with our data and hypothesis, as non-unique parallel substitutions could be generated by chance in any pair of mammals following phylogenetic distance.

Marine Mammals: Evolutionary Biology

Therefore, a combination of different evolutionary models, for example, the use of substitution rate and likelihood scores, as employed in the present study, may be necessary for future studies of convergent evolution. It should be noted that multiple factors, including genome size and complexity, may influence whether parallel mutations occur at the same nucleotide positions or in the same gene or complex locus In the case of marine mammals, there may be two additional factors that result in distinct substitutions in common genes.

First, terrestrial mammals returned to the sea at different evolutionary periods and, thus, under different genomic and environmental contexts. Second, it is clear that the adaptation to aquatic environments required multiple episodes of phenotypic convergence and likely involved multiple potentially adaptive mutations. Third, convergence generally involves four types of molecular evolution Although sequence convergence is the easiest to detect, other mechanisms functional, mechanistic and structural convergence may also play critical roles in the convergent evolution of marine mammals.

Two types of mutation changes which may correlate with the aquatic adaptation of marine mammals have not been interrogated in the present study: mutations in distinct genes associated with the same pathway and mutations in cis regulatory regions. For example, distantly-related electric fish show both sequence convergence 32 and mechanistic convergence in the form of common gene expression patterns enabling the development of electric organs In addition, regulatory mutations in PITX1 show signatures of positive selection in pelvic-reduced populations Future studies, for example functional or genomic analyses of non-coding regions, of marine mammals may complement our present study and provide further insights into the genomic basis of aquatic adaptations in mammals.

For genes with many reference sequences, the longest coding sequence was chosen. To confirm common changes in cetaceans that had not been included in the human UCSC species, coding sequences of the Yangtze River dolphin Lipotes vexillifer , assembly accession: GCA In order to conduct evolutionary model analyses, coding sequences from species shown in Fig. Cow Bos taurus, UMD3. To identify parallel amino acid changes in marine mammals, the phylogenetic tree of 62 mammals used for reconstruction of ancestral sequences was trimmed from the original tree, with branch length from the human UCSC species whole-genome multiple alignment.

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The ancestral sequences for each node were reconstructed with the help of FastML 3. We allowed FastML 3.

Amino acid changes of interest were manually validated. In the evolutionary analyses, coding sequences CDS of individual genes from the human genome were used to query the other 19 genomes listed in the Data collection section above and shown in Fig. Prior to using human genes to query genomes, we discarded sequences in which the CDS contained less than nucleotides and CDS length was not divisible by 3. For genes with alternatively spliced transcripts in the human genome, the CDS with the greatest number of nucleotides were used in further analyses.

The Rise of Marine Mammals

The branch site model 31 was used to detect positively selected genes in each marine lineage, respectively. A false discovery rate FDR, Bonferroni method correction was applied to account for multiple hypothesis testing. To detect signatures of molecular convergence, we fitted the orthologous CDS alignment data to a null model H 0 , species tree and an alternative model H A , the constraint of monophyly of marine mammals.

This method directly compares the goodness-of-fit of each gene to a pair of phylogenetic trees under a given model. We further estimated significance of convergence by performing analyses on simulated datasets. Fifty genes were randomly chosen to represent the alignment length and heterogeneity of our data. The simulations were carried out using Seq-Gen 1. The substitution model for each locus was determined by ProtTest 3. The substitution model did not have significant impact on the convergent genes in the present study.

In the comparison of alternative models convergent tree and null model species tree , we introduced 9 trees representing different topologies, but all supported the monophyly of marine mammals Supplementary Fig. The data presented in this study include genes identified from any pair of hypothesis tests between alternative tree and species tree with defined P less than 0.

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All gene groups are potentially informative despite lower rankings and serve to guide biological interpretation How to cite this article : Zhou, X. Convergent evolution of marine mammals is associated with distinct substitutions in common genes. Author Contributions X.

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For example, analysis of oxygen isotopes incorporated into fossil tooth enamel indicates whether these mammals foraged in and, therefore, ingested fresh water or sea water. Comparisons between groups are made to see if there are any common patterns, particularly relating to adaptations to aquatic life. Results show that aquatic characteristics evolved in mosaic patterns and that different morphological solutions to aquatic conditions were achieved separately in each of these groups.

Changes in the axial and appendicular skeleton assist with locomotion for aquatic foraging. Marine Mammals: Evolutionary Biology, 3rd Edition is a succinct, yet comprehensive textbook devoted to the evolution, systematics, morphology, physiology, ecology, and behavior of marine mammals. Earlier editions of this valuable work are considered required reading for all marine biologists concerned with marine mammals, and this ebook continues that tradition of excellence with updated citations and an expansion of nearly every chapter that includes full color photographs and distribution maps.

That said, Marine mammals: evolutionary biology 3rd edition will certainly be popular with all students, because it is clearly and concisely written, and intelligently illustrated. Berta et al. Your email address will not be published. Save my name, email, and website in this browser for the next time I comment.

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