Research ArticleEVOLUTIONARY BIOLOGY

Genomic and functional evidence reveals molecular insights into the origin of echolocation in whales

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Science Advances  03 Oct 2018:
Vol. 4, no. 10, eaat8821
DOI: 10.1126/sciadv.aat8821
  • Fig. 1 Detection of convergence between echolocating bats and ancestral whales.

    (A) Phylogeny of the mammalian species used to detect molecular convergence in this study. Bold lineages indicate toothed whales and echolocating bats with high-quality genomic data, and dashed lineages indicate the nonecholocating baleen whales and Old World fruit bats. The branches labeled I, II, III, IV, and V denote where convergent sites are counted. (B) Different comparisons of C/Ds of hearing-related genes based on the data set containing the inferred amino acids with ≥0.95 posterior probabilities. The numbers of convergent and divergent sites are given on the bars. C/D indicates the ratio of the number of convergent sites to the number of divergent sites. The P values are from two-tailed χ2 tests.

  • Fig. 2 Evolutionary convergence is significantly higher for hearing genes than for nonhearing genes between LCATW and echolocating bats.

    Frequency distributions of C/Ds from 104 genes unrelated to hearing for a total of 1000 random sets in the I and II (A), I and III (B), I and IV (C), and I and V (D) comparisons based on the data set containing the inferred amino acids with ≥0.95 posterior probabilities. The arrow in each panel indicates the ratio of the number of convergent sites to the number of divergent sites (C/D) identified from 104 hearing-related genes from different comparisons. C/D indicates the ratio of the number of convergent sites to the number of divergent sites.

  • Fig. 3 Functional results of prestin in modern whales.

    (A) Phylogenetic relationships of whales with prestin sequences. Species names in red indicate echolocating toothed whales, and those in blue denote nonecholocating whales. Underlined names are representative species chosen for the functional examination of their prestin genes. (B) Representative fitting curves of nonlinear capacitance obtained from human embryonic kidney (HEK) 293 cells transfected by prestin. Different line types and colors indicate different species. (C) Comparison of three functional parameters, 1/α, V1/2, and Qmax/Clin, between echolocating and nonecholocating whales. All values are presented as means ± SE. *P < 0.05, **P < 0.01, ***P < 0.001. All P values are from Student’s t tests.

  • Fig. 4 Plot of 1/α versus the frequency of best hearing sensitivity showing significant relationships (R = 0.77, P = 0.015, F test).

    Squares represent whale species, and circles represent other mammals. The squares in red indicate echolocating mammals, and those in blue denote nonecholocating mammals.

  • Fig. 5 Functional tests for resurrected ancestral prestin genes.

    (A) Schematic phylogenetic tree showing the nodes where ancestral prestin genes are examined. Representative fitting curves of NLC derived from ancestral prestins are shown. (B) Comparison of 1/α values of prestin among the ancestral and living whales as well as their outgroup. (C) Convergent sites (S392A and L497M) between the LCATW and echolocating bats account for enhancement of the functional parameter 1/α. Both convergent sites have mutations based on the prestin backgrounds of the LCAW and the LCATW, respectively. Values of 1/α significantly increase in the LCAW double mutant and decrease in the LCATW double mutant when compared to their respective wild-type controls. All values are given as means ± SE. **P < 0.01 and ***P < 0.001. All P values are from Student’s t tests.

  • Table 1 Top 10 of GO enrichment categories for convergent genes based on the PP0.95 data set.
    GO IDDescriptionP valueq value
    Enrichment analysis for the convergent genes between branches I and IV
    GO:0007283Spermatogenesis2.79E-050.0119
    GO:0048232Male gamete generation3.04E-050.0119
    GO:0009913Epidermal cell differentiation4.43E-050.0119
    GO:0060113Inner ear receptor cell differentiation4.50E-050.0119
    GO:0060119Inner ear receptor cell development6.79E-050.0147
    GO:0042490Mechanoreceptor differentiation1.24E-040.0241
    GO:0051321Meiotic cell cycle1.83E-040.0338
    GO:0030855Epithelial cell differentiation2.71E-040.0476
    GO:0008544Epidermis development3.19E-040.0486
    GO:0007605Sensory perception of sound3.30E-040.0486
    Enrichment analysis for the convergent genes between branches I and V
    GO:0060271Cilium morphogenesis9.66E-050.0523
    GO:0042384Cilium assembly2.19E-040.0833
    GO:0044782Cilium organization2.22E-040.0833
    GO:0003351Epithelial cilium movement3.93E-040.1131
    GO:0045766Positive regulation of angiogenesis4.24E-040.1133
    GO:0010927Cellular component assembly involved in morphogenesis5.30E-040.1322
    GO:0042312Regulation of vasodilation9.00E-040.2105
    GO:1904018Positive regulation of vasculature development1.25E-030.2531
    GO:0035082Axoneme assembly1.28E-030.2531
    GO:0007017Microtubule-based process1.49E-030.2539

Supplementary Materials

  • Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/full/4/10/eaat8821/DC1

    Fig. S1. Detection of convergence in hearing-related genes based on the PP0.7 data set.

    Fig. S2. Detection of convergence in hearing-related genes based on the PP0.5 data set.

    Fig. S3. The phylogenetic tree that we used to test whether the number of the observed convergent sites exceeds the neutral expectations.

    Table S1. Top 10 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.95 data set.

    Table S2. Hearing-related genes based on the annotations in the DAVID database.

    Table S3. Top 15 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.7 data set.

    Table S4. Top 15 of GO enrichment categories for convergent genes between branches I and IV and between branches I and V based on the PP0.7 data set.

    Table S5. Top 15 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.5 data set.

    Table S6. Top 15 of GO enrichment categories for convergent genes between branches I and IV and between branches I and V based on the PP0.5 data set.

    Table S7. Whale species used in this study.

  • Supplementary Materials

    The PDF file includes:

    • Fig. S1. Detection of convergence in hearing-related genes based on the PP0.7 data set.
    • Fig. S2. Detection of convergence in hearing-related genes based on the PP0.5 data set.
    • Fig. S3. The phylogenetic tree that we used to test whether the number of the observed convergent sites exceeds the neutral expectations.

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    Other Supplementary Material for this manuscript includes the following:

    • Table S1 (Microsoft Excel format). Top 10 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.95 data set.
    • Table S2 (Microsoft Excel format). Hearing-related genes based on the annotations in the DAVID database.
    • Table S3 (Microsoft Excel format). Top 15 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.7 data set.
    • Table S4 (Microsoft Excel format). Top 15 of GO enrichment categories for convergent genes between branches I and IV and between branches I and V based on the PP0.7 data set.
    • Table S5 (Microsoft Excel format). Top 15 of GO enrichment categories for convergent genes between branches I and II and between branches I and III based on the PP0.5 data set.
    • Table S6 (Microsoft Excel format). Top 15 of GO enrichment categories for convergent genes between branches I and IV and between branches I and V based on the PP0.5 data set.
    • Table S7 (Microsoft Excel format). Whale species used in this study.

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