1. Biochemistry and Chemical Biology
  2. Evolutionary Biology

Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision

  1. Gianni M Castiglione
  2. Belinda SW Chang  Is a corresponding author
  1. University of Toronto, Canada
https://doi.org/10.7554/eLife.35957
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Cite this article
  1. Gianni M Castiglione
  2. Belinda SW Chang
(2018)
Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision
eLife 7:e35957.
https://doi.org/10.7554/eLife.35957
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5 figures, 11 tables and 4 additional files

Figures

Figure 1 with 2 supplements
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Natural variation at site 122 determines rhodopsin function and stability.

(A) Amino acid consensus residues at site 122 across vertebrate rod opsins (rhodopsin; RH1) and the cone opsins (long-wave (LWS), short-wave (SWS1 and SWS2) and middle-wave (RH2) sensitive). Modified from (Lamb et al., 2007). (B) Relative stability of the rod and cone opsin active-conformation (MII) in different vertebrates (Imai et al., 2005). (C) Schematic representation of naturally occurring cone opsin variants (COVs) and other amino acids across vertebrate RH1 (see Figure 1—figure supplements 1–2; Tables 1–2, Supplementary files 1–2). E122 is invariant in all Tetrapod RH1 genes sequenced to date. Natural deep-sea amino acid variants (Hunt et al., 2001; Yokoyama et al., 1999) are identified with an asterisk (*; Table 2). (D) Introduction of the ancestral cone opsin (LWS) variant I122 blue shifts tetrapod RH1 spectral absorbance and accelerates decay of the MII light-activated conformation.

https://doi.org/10.7554/eLife.35957.003
Figure 1—figure supplement 1
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Schematic of RH1 site 122 variation across the vertebrate phylogeny.

All known tetrapod RH1 is conserved as E122. Asterisks indicate the presence of deep-dwelling species within a clade (Hunt et al., 2001; Yokoyama et al., 1999) (Table 2).

https://doi.org/10.7554/eLife.35957.004
Figure 1—figure supplement 2
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Vertebrate phylogeny used in computational analyses.

Tetrapods (green) and Teleost fishes (blue) along with outgroups (black) relationships were constructed according to species relationships (see Materials and methods).

https://doi.org/10.7554/eLife.35957.005
Figure 2 with 1 supplement
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Local coevolutionary forces govern the evolution of site 122 differentially between tetrapods and fish (teleost) RH1.

(A) Extant and reconstructed codon variation at site 122 (Materials and methods). Despite a variety of residues at site 122 across the Coelacanth (Q122), Lungfish (I122; Ceratodontiformes), and Tetrapods (E122), GAA codons encoding for E122 are nevertheless predicted as the ancestral state with high posterior probabilities (shown in parentheses). E122 (GAA/GAG) is also likely to have been present in the last common ancestor of Cypriniformes and the Characiphysi, although with low posterior probabilities and therefore high uncertainty. I122 codon ATC is fixed in all Characiphysi rhodopsin to our knowledge (Supplementary file 3). Approximate divergence times are from (Hedges et al., 2015). (B) Mutual information (MI) analyses (MISTIC [Simonetti et al., 2013]) reveal all sites coevolving with site 122 are within 6 Å. Significance thresholds were determined by reference to the highest MI z-score from all sites across analyses of randomized datasets (n = 150; z-score cut-off = 21.6), as previously described (Ashenberg and Laub, 2013). (C) Sites within this radius displayed decreased amino acid variation in tetrapod and characiphysi RH1, where E122 and I122 are fixed, respectively (asterisks). (D) In tetrapods and characiphysi RH1, reduction in amino acid variation (relative to teleosts) at positions within the 6 Å radius were driven by increases in purifying selection on non-synonymous codons. Statistically significant gene-wide increases in purifying selection (*) between lineages were detected by likelihood ratio tests of alternative (Clade model C [Bielawski and Yang, 2004]) and null (M2a_REL [Weadick and Chang, 2012]) model analyses of codon substitution rates (dN/dS) ((p<0.001); Tables 3–5). Sites estimated to be under this increase in purifying selection (*) were those identified in the divergent site class of the CmC model analyses through a Bayes empirical Bayes analysis as previously described (Castiglione et al., 2017. Site-specific dN/dS estimates are from M8 analyses on phylogenetically pruned datasets (Tables 8–10; Figure 1—figure supplement 2; Figure 2—figure supplement 1).

https://doi.org/10.7554/eLife.35957.008
Figure 2—figure supplement 1
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Phylogeny used in PAML computational analyses of Characiphysi rhodopsin coding-sequences, along with outgroups (Table 10; Supplementary file 3).

Relationships were constructed according to species relationships (see Materials and methods).

https://doi.org/10.7554/eLife.35957.009
Figure 3
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Coevolving sites form the LxxEIA and FxxINS motifs.

(A) Overview of tetrapod RH1 MII rhodopsin crystal structure (Choe et al., 2011 with coevolving sites. The green highlight and dashed line indicate the stabilizing hydrogen bond between E122-H211. (B) Reconstruction of residues at site 122 (Figure 2—figure supplement 1) and coevolving positions for ancestral characiphysi, tetrapod and outgroup rhodopsins indicates the entrenchment of two structural motifs centering around site 122 (Materials and methods). The LxxEIA (or LEIA) motif was also predicted as present within the ancestral Osteichthyes. Approximate divergence times are from (Hedges et al., 2015.

https://doi.org/10.7554/eLife.35957.013
Figure 4 with 1 supplement
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Coevolving sites modulate the pleiotropic functional effects of site 122.

The LEIA and FINS motifs are convergent solutions for high tetrapod RH1 active state (MII) stability but with different spectral absorbances. (A) The introduction of the ancestral cone opsin variant into tetrapod RH1 (E122I) blue-shifts rhodopsin absorbance λMAX and dramatically destabilizes the MII active-conformation (Figure 4—figure supplement 1; Table 6). Bar graphs show retinal release half-life values. (B) Substituting FINS motif residues into coevolving sites have varied effects on rhodopsin spectral tuning and the stability of the active-conformation. (C) Within the E122I background, FINS motif substitutions at coevolving sites have marked effects on spectral tuning, but no rescue effect on MII active-conformation stability. (D) Partial incorporation of the FINS motif within tetrapod rhodopsin produces further blue-shifting effects and has a significant but small stabilizing effect within the E122I background. (E) Full incorporation of the FINS motif into tetrapod RH1 maintains the absorbance blue-shift while fully rescuing the destabilizing effects of E122I on tetrapod RH1. Statistically significant differences in MII stability were calculated using two-tailed t-tests with unequal variance, with standard error reported in bar graphs (*p<0.05; **p<0.01; ***p<0.001). The number of biological replicates (i.e. separate elutions and/or purifications of rhodopsin) are described in Table 6.

https://doi.org/10.7554/eLife.35957.014
Figure 4—figure supplement 1
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Absorbance spectra of dark-state WT and mutant rhodopsins with wavelength of maximum absorbance (λMAX) shown.
https://doi.org/10.7554/eLife.35957.015
Figure 5 with 1 supplement
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LEIA and FINS motifs are alternative solutions for high tetrapod RH1 MII stability within a limited sequence-function landscape.

Spectral absorbance (λMAX) and stability of the active-conformation (MII) of wild type and mutant tetrapod RH1 with E122 (green) and I122 (blue), respectively. The only natural intermediate between the wild-type tetrapod consensus motif (LEIA) and the wild-type Characiphysi motif (FINS) is ‘FIIA’ from Lungfish RH1. The mutation I123N has opposite effects on MII stability depending on background sequence (sign-epistasis), which may have closed the LEIA to FINS motif evolutionary trajectory (dashed line) for tetrapod RH1.Although reflecting a limited experimental dataset, these epistatic effects may have created indirect routes to the high MII stability of the FINS motif via intermediates with low MII stability.

https://doi.org/10.7554/eLife.35957.017
Figure 5—figure supplement 1
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Compensatory effects at coevolving sites are mediated by a diversity of possible structural mechanisms.

(A) Overview of a homology modeled mutant rhodopsin MII structure containing the FINS motif (Materials and methods) (Choe et al., 2011. F119 is membrane-facing (blue). (B) Zoom-in of F119 and buried-site N123, which may form novel hydrogen bonds with nearby conserved residues N78 and T160. These interactions may alter the conformation of residues near S124, as shown in (C) where D83, S298 and N302 participate in a hydrogen bond network stabilizing the active-conformation (Choe et al., 2011). Cascading structural alterations from F119, to N123 to S124 (green) may therefore increase active-conformation stability by integrating into existing stabilizing motifs, therefore compensating for the loss of the E122-H211 hydrogen bond (red).

https://doi.org/10.7554/eLife.35957.018

Tables

Table 1
Variation at sites 119-122-123-124 in Tetrapods and Outgroup rh1.

Sites with variation relative to the Vertebrate consensus (LEIA) are in bold and highlighted grey. Subterranean species are denoted (*).

https://doi.org/10.7554/eLife.35957.006
SpeciesAccessionCommon name119122123124
OutgroupsCallorhinchus miliiXP_007888679Elephant sharkLEIG
Orectolobus ornatusAFS63882Ornate wobbegongLEVS
Latimeria chalumnaeXP_005997879CoelacanthLQVA
Neoceratodus forsteriABS89278Australian lungfishFIIA
MammalsDasypus novemcinctusXP_0044773039-banded armadillo*IEIA
Eptesicus fuscusXP_008150514Big brown batLEVA
Chrysochloris asiaticaXP_006868732Cape golden mole*MEIA
Sorex araneusXP_004613289Common Shrew*LEVA
Tupaia chinensisXP_006160726Tree ShrewLEVA
Ictidomys tridecemlineatusXP_00533384113-line ground squirrelLEVA
Rattus norvegicusNP_254276brown ratLEIG
Sarcophilus harrisiiXP_003762497Tasmanian devilTEVA
ReptilesAlligator mississippiensisXM_006274155American alligatorLEVA
Alligator sinensisXP_006039462Chinese alligatorLEVA
Anolis carolinensisNP_001278316Carolina anoleLEMG
Python bivittatusXP_007423324Burmese pythonLEMA
AmphibiansAmbystoma tigrinumU36574Tiger salamanderMEIA
Cynops pyrrhogasterBAB55452Jap. Fire belly newtLEIG
Xenopus tropicalisNP_001090803Western clawed frogLEMA
Xenopus laevisNP_001080517African clawed frogLEVA
Table 2
Fish rh1 with variation at site 122 do not necessarily have variation at coevolving sites 119, 123, and 124.

Sites with variation relative to the Vertebrate consensus (LEIA) are in bold and highlighted grey.

https://doi.org/10.7554/eLife.35957.007
OrderSpeciesAccessionCommon name119122123124Ecology notes from FishBase
LepisosteiformesLepisosteus oculatusJN230969.1spotted garLMISFreshwater; brackish; demersal. (Ref. 2060)
Atractosteus tropicusJN230970.1Tropical GarLMLSFreshwater; demersal
OsteoglossiformesMormyrops anguilloidesJN230973.1Cornish JackTIIAFreshwater; demersal; potamodromous (Ref. 51243)
Osteoglossum bicirrhosumKY026030.1Silver arowanaTIIAFreshwater; benthopelagic
 AlepocephalifromesAlepocephalus bicolorJN230974.1Bicolor slickheadLQIAMarine; bathydemersal; depth range 439–1080 m (Ref. 44023).
Bathytroctes microlepisJN544540.1Smallscale smooth-headLDIAMarine; bathypelagic; depth range 0–4900 m (Ref. 58018)
Conocara salmoneumJN412577.1Salmon smooth-headLQIAMarine; bathypelagic; depth range 2400–4500 m (Ref. 40643)
 GalaxiiformesGalaxias maculatusJN231000.1InangaLMIGMarine; freshwater; brackish; benthopelagic; catadromous (Ref. 51243).
StomiatiformesArgyropelecus aculeatusJN412571.1Lovely HatchetfishHQIAMarine; bathypelagic; depth range 100–2056 m (Ref. 27311)
Vinciguerria nimbariaJN412570.1Oceanic lightfishHQVAMarine; bathypelagic; depth range 20–5000 m (Ref. 4470)
 AteleopodiformesAteleopus japonicusKC442218.1Pacific Jellynose FishLMISMarine; bathydemersal; depth range 140–600 m (Ref. 44036).
 MyctophiformesBenthosema suborbitaleJN412576.1Smallfin lanternfishHQVGMarine; bathypelagic; oceanodromous; depth range 50–2500 m (Ref. 26165)
Lampanyctus alatusJN412575.1Winged lanternfishHQVAMarine; bathypelagic; oceanodromous; depth range 40–1500 m (Ref. 26165)
Neoscopelus microchirKC442224.1Shortfin neoscopelidLQIAMarine; bathypelagic; depth range 250–700 m (Ref. 4481)
GadiiformesCoryphaenoides guentheriJN412578.1Gunther’s grenadierLVIAMarine; bathydemersal; depth range 831–2830 (Ref. 1371)
 BeryciformesMelamphaes suborbitalisJN231006.1Shoulderspine bigscaleLQIAMarine; brackish; bathypelagic; depth range 500–1000 m (Ref. 31511).
HolocentriformesHolocentrus rufusKC442230.1Longspine squirrelfishLMISMarine; reef-associated; depth range 0–32 m (Ref. 3724).
Myripristis murdjanKC442231.1Pinecone soldierfishLMIGMarine; reef-associated; depth range 1–50 m (Ref. 9710)
 ScombriformesAphanopus carboEU637938.1Black scabbardfishHQIGMarine; bathypelagic; oceanodromous (Ref 108735); 200–2300 m (Ref. 108733)
Cubiceps gracilisEU637952.1Driftfish-QIAMarine; pelagic-oceanic; oceanodromous (Ref. 51243);
Table 3
Results of Clade Model C (CmC) analyses of vertebrate rh1 under various partitions.
https://doi.org/10.7554/eLife.35957.010
Model and
Foreground†		ΔAIC‡lnLParametersNullP [df]
ω0ω1ω2/ωd
 M2a_rel225.5−47185.370.02 (69%)1 (3%)0.20 (28%)N/A-
CmC_Tetrapod Branch97.44−47119.330.20
(28%)		1
(3%)		0.02 (69%)
Tetra Br: 0.00		M2a_rel0.000 [1]
CmC_Tetrapod4.92−47073.060.02 (67%)1 (3%)0.24 (30%)
Tetra: 0.13		M2a_rel0.000 [1]
CmC_Teleost1.88−47071.540.02 (67%)1 (3%)0.14 (30%)
Teleost: 0.24		M2a_rel0.000 [1]
CmC_Teleost vs Tetrapod0*−47069.600.02 (67%)1 (3%)0.17 (30%)
Tetra: 0.13
Teleost: 0.24		M2a_rel0.000 [2]

  1. †The foreground partition is listed after the underscore for the clade models and consists of either: the clade of Teleost fishes (Teleost); the clade Tetrapods (Tetrapod;Tetra) or branch leading to tetrapods (Tetrapod branch; Tetra Br); or the clades of both the teleost fishes and tetrapods as two separate foregrounds (Teleost vs Tetrapods). In any partitioning scheme, the entire clade was tested, and all non-foreground data are present in the background partition.

    ‡All ΔAIC values are calculated from the lowest AIC model. The best fit is shown with an asterisk (*).

  2. ωd is the divergent site class, which has a separate value for the foreground and background partitions.

    Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  3. Abbreviations—lnL, ln Likelihood; p, p-value; AIC, Akaike information criterion.

Table 4
Analyses used to elucidate sites coevolving with site 122 in Vertebrate rhodopsins (rh1).

In bold are the results of interest described in the main text, including: elevated dN/dS, long-term shifts in selection between teleosts and tetrapods, amino acid statistical covariation with site 122 in the teleost dataset, and phylogenetically correlated amino acid variation with site 122.

https://doi.org/10.7554/eLife.35957.011
SiteDistance to site 122 (Å)*Tetrapod M8 dN/dS†Teleost M8 dN/dS†Characiphysi M8 dN/dS†Posterior probability of long-term shift in selection
(tetrapod/characiphysi)‡		Z-score covariation§Significant correlated evolution?
11850.050.050.050.00/0.00−1.54No
1193.50.140.1680.050.57/0.1930.2Yes
1203.10.050.050.050.00/0.00−1.91No
121N/A0.050.050.050.00/0.00−0.94No
122N/A0.050.3220.051.00/1.00N/AN/A
123N/A0.190.0940.050.00/0.0020.4No
1243.20.050.4110.051.00/1.005.53No
1253.40.050.050.050.00/0.001.19No
1263.70.050.050.050.00/0.00−1.60No
1274.90.050.0650.050.00/0.0027.1Yes
1605.10.050.050.050.00/0.003.90No
1644.20.050.050.050.00/0.007.88No
1673.80.050.050.050.00/0.00−1.38No
1685.90.050.3080.1921.00/1.0034.2No
2074.90.050.050.050.00/0.00−1.21No
2112.70.050.050.050.00/0.00−1.38No
2655.10.050.050.050.00/0.00−1.44No

  1. ∗From structural analysis of distances between amino acids and site 122 within the MII crystal structure 3PQR (Choe et al., 2011).

    †Post mean dN/dS from M8 analyses described in Tables 8–10.

  2. ‡Bayes empirical Bayes posterior probability of long-term shift in selection calculated in Clade model C (CmC) (Yang, 2007) analyses (CmC_Teleost vs Tetrapod/CmC_Characi clade) described in Tables 3 and 5, respectively.

    §Phylogenetically corrected MI z-scores (MISTIC; [Simonetti et al., 2013]) of covariation with site 122 from analyses on Teleost RH1 dataset. Values were considered significant if greater than the top absolute z-score (21.6) from all site-wise comparisons from all analyses of 150 randomized datasets, as described (Ashenberg and Laub, 2013).

  3. Tests of correlated evolution in amino acid variation (Pagel, 1994) between a given site and site 122. p-values were calculated by performing Monte Carlo tests using data from simulations (n > 1000) in MESQUITE (Maddison and Maddison, 2017). p-Values were subjected to a Bonferroni-correction to determine significance (p<0.002).

Table 5
Results of Clade Model C (CmC) analyses of teleost rh1 under various partitions. 
https://doi.org/10.7554/eLife.35957.012
Model and
Foreground†		ΔAIC‡lnLParametersNullP [df]
ω0ω1ω2/ωd
M2a_rel17.1−30987.990.01 (60%)1 (5%)0.19 (35%)N/A-
CmC_Characi branch19.05−30986.960.01 (60%)1 (5%)0.19 (35%)
Char Br: 0.20		M2a_rel0.794 [1]
CmC_Characi clade0*−30977.430.00 (60%)1 (5%)0.20 (20%)
Char Cl: 0.10		M2a_rel0.000 [1]

  1. The foreground partition is listed after the underscore for the clade models and consists of either: the ancestral branch leading to the Characiphysi (Characi branch; Char Br) or the entire Characiphysi clade (Characi clade; Char Cl). In any partitioning scheme, the entire clade was tested, and all non-foreground data are present in the background partition.

    ‡All ΔAIC values are calculated from the lowest AIC model. The best fit is bolded with an asterisk (*).

  2. §ωd is the divergent site class, which has a separate value for the foreground and background partitions.

    Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  3. Abbreviations—lnL, ln Likelihood; p, p-value; AIC, Akaike information criterion.

Table 6
Summary of spectroscopic assays on wild-type and mutant rhodopsins.
https://doi.org/10.7554/eLife.35957.016
119-122-123-124 motifλMAX (nm)∗,†Half-life of retinal release1,2
Wild-type Bovine rhodopsinLEIA498.2 ± 0.1 (4)13.3 ± 0.6 (4)
L119FFEIA503.5 ± 0.8 (3)17.4 ± 0.8 (3)
E122ILIIA495.4 ± 0.2 (4)5.93 ± 0.6 (3)
I123NLENA498.0 ± 0.3 (3)7.31 ± 0.9 (4)
A124SLEIS496.6 ± 0.2 (3)23.5 ± 0.4 (3)
L119F/E122IFIIA496.6 ± 0.4 (3)7.68 ± 0.3 (3)
E122I/I123NLINA494.86.47 ± 0.3 (3)
E122I/A124SLIIS492.5 ± 0.5 (3)7.24 ± 0.2 (3)
L119F/E122I/A124SFIIS492.2 ± 0.1 (3)9.40 ± 0.2 (3)
L119F/E122I/I123N/A124SFINS492.6 ± 0.3 (4)15.7 ± 0.8 (3)

  1. ∗Standard error is shown.

    †Number of biological replicates (i.e. separate elutions and/or purifications of rhodopsin) is shown in brackets.

Key resources table
Reagent type
(species) or resource		DesignationSource or referenceIdentifiersAdditional
information
 gene
(Bos taurus)		RH1(Rho)N/AAccession: M12689
 cell line
(Homo sapiens)		HEK293TDr. David Hampson, University of TorontoAuthenticated
by STR profiling
 transfected
construct		pIRES-hrGFP IIStratagene
 antibody1D4 monoclonal antibodydoi: 10.1007/978-1-4939-1034-2_1fixed to Ultralink
Resin (5mg 1D4:7mL Resin)
 commercial
assay or kit		Lipofectamine 2000ThermoFisher ScientificCatalog Number: 11668019
Commercial
assay or kit		Ultralink Hydrazide ResinThermoFisher ScientificCatalog Number: 53149
Chemical
compound, drug		11-cis retinalotherDr. Rosalie Crouch, Medical University
of South Carolina
 sSoftware,
algorithm		PAML 4.7https://doi.org/10.1093/molbev/msm088
 sSoftware,
algorithm		MISTICdoi: 10.1093/nar/gkt427
Software,
algorithm		MODELLERdoi: 10.1002/cpbi.3
Table 7
Analyses of selection on Vertebrate rhodopsin (rh1) using PAML random sites models.
https://doi.org/10.7554/eLife.35957.019
ModellnLParameters1NullP [df]2Δ AIC§
ω0/pω1/qω2/ωp
M0−49624.890.08--N/A-5516.80
M1a−48355.440.05 (89%)1.00 (11%)-M00.000 [1]2979.91
M2a−48355.440.05 (89%)1.00 (3%)1.00 (8%)M1a1 [2]2983.91
M3−47104.840.01 (58%)0.11 (30%)0.44 (12%)M00.000 [4]484.71
M7−46906.240.241.19-N/A-81.51
M8a−46864.600.323.101.00N/A-0.230
M8−46863.490.322.941.14M70.000 [2]0*
M8a0.135 [1]

  1. 1ω values of each site class are shown are shown for model M0-M3 (ω0– ω2) with the proportion of each site class in parentheses. For M7 and M8, the shape parameters, p and q, which describe the beta distribution are listed instead. In addition, the ω value for the positively selected site class (ωp, with the proportion of sites in parentheses) is shown for M8.

    2Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  2. 3#Model fits were assessed by Akaike information criterion differences to the best fitting model (asterisk).

    Abbreviations—lnL, ln Likelihood; p, p-value; N/A, not applicable.

Table 8
Analyses of selection on Teleost rhodopsin (rh1) using PAML random sites models.
https://doi.org/10.7554/eLife.35957.020
ModellnLParameters1† NullP [df]†Δ AIC§
ω0/pω1/qω2/ωp
M0−32949.460.10--N/A-4489.79
M1a−31605.100.05 (86%)1.00 (14%)-M00.000 [1]1803.10
M2a−31605.100.05 (86%)1.00 (10%)1.00 (4%)M1a1 [2]1807.10
M3−30887.400.01 (58%)0.13 (29%)0.57 (13%)M00.000 [4]373.67
M8a−30790.440.283.051.00N/A-173.76
M7−30767.110.190.68-N/A-127.10
M8−30702.570.251.621.92M70.000 [2]0*
M8a0.000 [1]

  1. 1ω values of each site class are shown are shown for model M0-M3 (ω0– ω2) with the proportion of each site class in parentheses. For M7 and M8, the shape parameters, p and q, which describe the beta distribution are listed instead. In addition, the ω value for the positively selected site class (ωp, with the proportion of sites in parentheses) is shown for M8.

    2Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  2. 3#§Model fits were assessed by Akaike information criterion differences to the best fitting model (asterisk).

    Abbreviations—lnL, ln Likelihood; p, p-value; N/A, not applicable.

Table 9
Analyses of selection on Tetrapod rhodopsin (rh1) using PAML random sites models.
https://doi.org/10.7554/eLife.35957.021
ModellnLParameters† NullP [df]‡Δ AIC§
ω0/pω1/qω2/ωp
M0−15541.640.05--N/A-1154.78
M1a−15345.330.03 (93%)1.00 (7%)-M0[1]764.17
M2a−15345.330.03 (93%)1.00 (0%)1.00 (7%)M1a1 [2]768.17
M3−14981.400.00 (61%)0.06 (28%)0.29 (11%)M00.000 [4]42.31
M7−14971.780.192.76-N/A-17.10
M8−14961.250.203.551.00M70.000 [2]0*

  1. 1ω values of each site class are shown are shown for model M0-M3 (ω0– ω2) with the proportion of each site class in parentheses. For M7 and M8, the shape parameters, p and q, which describe the beta distribution are listed instead. In addition, the ω value for the positively selected site class (ωp, with the proportion of sites in parentheses) is shown for M8.

    2Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  2. 3#Model fits were assessed by Akaike information criterion differences to the best fitting model (bolded asterisk).

    Abbreviations—lnL, ln Likelihood; p, p-value; N/A, not applicable.

Table 10
Analyses of selection on Characiphysi rhodopsin (rh1) using PAML random sites models.
https://doi.org/10.7554/eLife.35957.022
ModellnLParameters1NullP [df]2Δ AIC§
ω0/pω1/qω2/ωp
M0−10819.130.06--N/A-842.6
M1a−10586.680.03 (91%)1.00 (9%)-M00.000 [1]379.73
M2a−10586.680.03 (91%)1.00 (9%)9.07 (0%)M1a1 [(2383.7
M3−10403.200.00 (60%)0.08 (29%)0.40 (11%)M00.000 4)18.8
M7−10401.450.171.77-N/A-9.27
M8a−10395.820.182.271.00N/A-0.23
M8−10394.820.182.221.50M70.000 (2]0*
M8a0.136 [1]

  1. ∗†ω values of each site class are shown are shown for model M0-M3 (ω0– ω2) with the proportion of each site class in parentheses. For M7 and M8, the shape parameters, p and q, which describe the beta distribution are listed instead. In addition, the ω value for the positively selected site class (ωp, with the proportion of sites in parentheses) is shown for M8.

    ‡Significant p-values (α ≤0.05) are bolded. Degrees of freedom are given in square brackets after the p-values.

  2. Model fits were assessed by Akaike information criterion differences to the best fitting model (asterisk).

    Abbreviations—lnL, ln Likelihood; p, p-value; N/A, not applicable.

Additional files

Supplementary file 1

Tetrapods and non-tetrapod Sarcopterygian outgroups with their respective rhodopsin coding-sequence (rh1) accession numbers.

https://doi.org/10.7554/eLife.35957.023
Supplementary file 2

Teleost fishes and cartilaginous outgroups with their respective rhodopsin coding-sequence (rh1) accession numbers.

https://doi.org/10.7554/eLife.35957.024
Supplementary file 3

Characiphysi (Siluriformes, Gymnotiformes, and Characiformes) with Cypriniforme outgroups with their respective rhodopsin coding-sequence (rh1) accession numbers.

https://doi.org/10.7554/eLife.35957.025
Transparent reporting form
https://doi.org/10.7554/eLife.35957.026

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  1. Gianni M Castiglione
  2. Belinda SW Chang
(2018)
Functional trade-offs and environmental variation shaped ancient trajectories in the evolution of dim-light vision
eLife 7:e35957.
https://doi.org/10.7554/eLife.35957