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Adaptation of mammalian myosin II sequences to body mass

Mark N Wass*1, Sarah T Jeanfavre*1,2, Michael P Coghlan*1, Martin Ridout#, Anthony J Baines*3 and Michael A Geeves*3 School of Biosciences*, and School of Mathematics#, Statistics and Actuarial Science, University of Kent, Canterbury, UK

1. Equal contribution 2. Current address: Broad Institute, 415 Main Street, 7029-K, Cambridge MA 02142 3. Joint corresponding authors

Key words: selection, muscle contraction, mammalian physiology, heart rate Address for correspondence: Prof M.A.Geeves School of Biosciences, University of Kent, Canterbury CT1 7NJ UK [email protected] tel 44 1227827597

Dr A J Baines School of Biosciences, University of Kent, Canterbury CT1 7NJ UK [email protected] tel 44 1227 823462 SUPPLEMENTARY MATERIAL

Supplementary Table 1. Source of Myosin sequences and the mass of each species used in the analysis of Fig 1 & 2

Species Isoform Mass Skeletal Skeletal Embryonic Skeletal α- β-cardiac Perinatal Non- Non- Smooth Extraocular Slow (kg) 2d/x 2a 2b cardiac muscle A muscle B Muscle Tonic Human P12882 Q9UKX2 251757455 Q9Y623 P13533 P12883 P13535 P35579 219841954 13432177 110624781 599045671 68a Bonobo 675746236 397494570 675746242 675746226 397473260 397473262 675746209 675764569 675746138 675746206 675798456 45.5a Macaque 544497116 544497114 544497126 109113269 544446347 544446351 544497122 383408157 384940798 387541766 544497107 544465262 6.55b 640786419 640786435 640786417 640818214 640818212 640786413 640796733 640805785 640786411 640822915 0.1315c Rat 205830438 G3V6E1 6981234 Q29RW1 P02563 P02564 F1M8F6 Q62812 Q9JLT0 282158051 F1M789 211938461 0.325b Mouse Q5SX40 G3UW82 153792649 Q5SX39 Q02566 Q91Z83 P13542 Q8VDD5 Q61879 20070691 124486959 145864471 0.017b Guinea 348560933 D6N3E0 524926861 348577524 348577522 348560930 348569442 514454472 H0VCX1 348560928 514456949 0.9a Hamster 348560937 514454246 P13539 P13540 524926859 524925525 524926815 524926855 0.1125a Cow Q9BE40 Q9BE41 156120319 E1BP87 O97496 Q9BE39 F1N775 F1MQ37 554569298 151554905 741963173 741948777 755a Brandt’s 554569234 554569240 554569232 554581513 554581511 554569226 G1PWB8 Q27991 554569314 554572455 0.0069b Minke 594653830 511880634 594665031 594653837 594622148 594623548 594681427 594692255 9200d 126308741 126308745 126308751 126308737 611969297 126277437 126308731 126339824 611994225 126334598 611994046 F7GF97 0.048b 1 2 3 4 6 7 8 9 10 11 13 7b Myosin Heavy Chain - MyHC

a = Diversity Web: animaldiversity.org b = ARKive: Arkive.org c = Primatology.net d= National Oceanic and Atmospheric Administration Fisheries: nmfs.noaa.gov

Sequence identifiers beginning with an upper case letter are from Uniprot. Identifiers consisting solely of numbers are NCBI GI numbers for Refseq Protein database entries.

Table S2 Source of Myosin sequences and the mass of each species used in the analysis of Figs 3-5 MyHC3 MyHC7 MyHC9 Weight Animal Organism (kg) Accession Accession Accession Orycteropus afer afer 61 XP_007949396.1| XP_007952162.1 African Elephant Loxodonta africana 4800 Afrotheria XP_010597690.1 pacos 60 Laurasiatheria XP_006216239.1 XP_006207100.1 American Pika Ochotona princeps 0.1485 XP_004589604.1 Dasypus novemcinctus 5.5 Metaferia XP_004483195.1 Bactrian Camelus bactrianus 475 Laurasiatheria XP_010964285.1 XP_010958676.1 Big Brown Bat Eptesicus fuscus 0.023 Laurasiatheria XP_008151670.1 XP_008142904.1 Bison bison bison 600 Laurasiatheria XP_010841308.1 Black Flying alecto 0.74 Laurasiatheria XP_006922456.1 XP_006913644.1 XP_006914548.1 Bolivian Squirrel Monkey Saimiri boliviensis boliviensis 0.75 Euarchontoglires XP_010341809.1 Bonobo Pan paniscus 44 Euarchontoglires XP_008969597.1 XP_003808134.1 XP_008973255.1 Brandts Bat Myotis brandtii 0.0069 Laurasiatheria XP_005878881.1 XP_005882279.1 XP_005883308.1 Camel Camelus ferus 800 Laurasiatheria XP_006181417.1 XP_006172852.1 XP_006194713.1 Cape Elephant edwardii 0.0695 Afrotheria XP_006890222.1 Cape Golden Chrysochloris asiatica 0.042 Afrotheria XP_006865288.1 taurus 755 Laurasiatheria NP_001095305.1 NP_777152.1 NP_001179691.1 Chinchilla Chinchilla lanigera 0.65 Euarchontoglires XP_005399419.1 XP_013366946.1 Chinese Hamster Cricetulus griseus 0.02235 Euarchontoglires XP_007630255.1* XP_007609272.1 XP_007622799.1 Chinese Tree Shrew Tupaia chinensis 0.16 Euarchontoglires XP_006156482.1 Colobus Colobus angolensis palliatus 8.9 Euarchontoglires XP_011788651.1 XP_011786220.1 XP_011819709.1 araneus 0.0095 Laurasiatheria XP_004603954.1 Coquerels Mouse Lemur Propithecus coquereli 0.305 Euarchontoglires XP_012509396.1 XP_012493546.1 Crab-Eating Macaque Macaca fascicularis 6.55 Euarchontoglires XP_005582959.1 XP_005560929.1 XP_005567470.1 Damaraland Mole- Rat Fukomys damarensis 0.144 Euarchontoglires XP_010613296.1 XP_010612194.1 David's Myotis Myotis davidii 0.0085 Laurasiatheria XP_006757501.1 Degu Octodon degus 0.235 Euarchontoglires XP_004645229.1 XP_004646724.1 XP_004634632.1 lupus familiaris 35.5 Laurasiatheria XP_005619582.1 NP_001107183.1 NP_001104237.1 Lipotes vexillifer 104.5 Laurasiatheria XP_007457908.1 XP_007449624.1 XP_007446800.1 Domestic catus 4.75 Laurasiatheria XP_011287146.1 XP_011281445.1 Drill Mandrillus leucophaeus 18.25 Euarchontoglires XP_011828556.1 XP_011834336.1 Camelus dromedarius 495 Laurasiatheria XP_010986392.1 XP_010997289.1 Mustela putorius furo 1.5 Laurasiatheria XP_004760220.1 Flying Lemur Galeopterus variegatus 1.45 Euarchontoglires XP_008564810.1 XP_008585579.1 Galago Otolemur garnettii 0.1025 Euarchontoglires XP_012661460.1 XP_012656616.1 melanoleuca 102.5 Laurasiatheria XP_002921226.1 XP_011217103.1 Gibbon Nomascus leucogenys 5.7 Euarchontoglires XP_012356893.1 hircus 45 Laurasiatheria XP_005680817.1 Golden Hamster Mesocricetus auratus 0.099 Euarchontoglires *P13540.2 Golden Snub-nosed Monkey Rhinopithecus roxellana 16.4 Euarchontoglires XP_010387470.1 Gray Mouse Lemur Microcebus murinus 0.06 Euarchontoglires XP_012642489.1 Green Monkey Chlorocebus sabaeus 5 Euarchontoglires XP_008008568.1 XP_007989071.1 XP_007973837.1 Ground Squirrel Ictidomys tridecemlineatus 0.125 Euarchontoglires XP_005332936.1 XP_005322354.1 Guinea Pig Cavia porcellus 0.9 Euarchontoglires XP_003466269.1 XP_003474533.1 XP_003470507.1 europaeus 0.6 Laurasiatheria XP_007522826.1 XP_007519425.1 caballus 563.5 Laurasiatheria XP_001504905.2 NP_001075227.1 Human Homo sapiens 68 Euarchontoglires NP_002461.2 NP_000248.2 NP_002464.1 Jerboa Jaculus jaculus 0.6 Euarchontoglires XP_004663184.1 XP_004650327.1 Kangaroo Rat Dipodomys ordii 0.0755 Euarchontoglires XP_012868629.1 XP_012880785.1 XP_012880308.1 Orcinus orca 7200 Laurasiatheria XP_004266884.1 XP_004283261.1* XP_004279478.1 Large Fruit Bat Pteropus vampyrus 0.85 Laurasiatheria XP_011357263.1 XP_011371126.1 XP_011385610.1 Little Brown Bat Myotis lucifugus 0.008 Laurasiatheria XP_006099793.1 XP_006100103.1 Trichechus manatus Manatee latirostris 480 Afrotheria XP_004390599.1 Mangabey Cercocebus atys 9.5 Euarchontoglires XP_011943848.1 Marmoset Callithrix jacchus 0.33 Euarchontoglires XP_002806839.1 XP_002753688.1 XP_009008395.1 acutorostrata scammoni 9200 Laurasiatheria XP_007175343.1 XP_007180640.1 XP_007165739.1 Mole-Rat Nannospalax galili 0.375 Euarchontoglires XP_008853933.1 XP_008838094.1 XP_008853014.1 Mouse Mus musculus 0.017 Euarchontoglires NP_001093105.1 NP_542766.1 NP_071855.2 Night monkey Aotus nancymaae 0.75 Euarchontoglires XP_012322603.1 XP_012331782.1 Olive Baboon Papio anubis 19.5 Euarchontoglires XP_009187946.1 XP_009215489.1 Opossum Monodelphis domestica 0.048 XP_001371653.1 XP_001369357.1 XP_001376000.1 Pig Sus scrofa 169 Laurasiatheria NP_999020.1 Pig-tailed macaque Macaca nemestrina 6.55 Euarchontoglires XP_011770587.1 XP_011710795.1 Platypus Ornithorhynchus anatinus 1.65 ** XP_003430622.1 Peromyscus maniculatus Prairie Mouse bairdii 0.017 Euarchontoglires XP_006973571.1 XP_006991969.1 Prairie Vole Microtus ochrogaster 0.05 Euarchontoglires XP_005349905.1 XP_013204243.1 Przewalskis Horse Equus przewalskii 250 Laurasiatheria XP_008527759.1 Rabbit Oryctolagus cuniculus 2 Euarchontoglires NP_001182585.1 XP_002718130.1 XP_008255309.1 Rat Rattus norvegicus 0.325 Euarchontoglires NP_036736.1 XP_006252013.1 NP_001292806.1 Rhesus Macaque Macaca mulatta 8 Euarchontoglires XP_001114005.2* Sheep aries 110 Laurasiatheria XP_004010374.1 XP_012004193.1 Siberian tigris altaica 176.4 Laurasiatheria XP_007086007.1 XP_007098159.1 Sooty Mangabey Cercocebus atys 9.5 Euarchontoglires XP_011906114.1 XP_011893491.1 Star Nosed Mole Condylura cristata 0.055 Laurasiatheria XP_004684642.1 Sumatran Orangutan Pongo abelii 60 Euarchontoglires XP_009232594.1 Tarsier Tarsius syrichta 0.1315 Euarchontoglires XP_008048958.1 XP_008065968.1 Pantholops hodgsonii 33 Laurasiatheria XP_005959866.1 Odobenus rosmarus divergens 1050 Laurasiatheria XP_004398481.1 XP_004417395.1 bubalis 725 Laurasiatheria XP_006055107.1 XP_006080999.1 XP_006057029.1 Leptonychotes weddellii 500 Laurasiatheria XP_006744844.1 Ceratotherium simum White Rhino simum 2520 Laurasiatheria XP_004433113.1 XP_004418151.1 Bos mutus 562.5 Laurasiatheria XP_005907260.1 XP_005909865.1

* The sequence for the Golden hamster came from Uniprot all other were accessed from Ref Seq ** The Clade for the Platypus is not well defined. Mass data came from the same sources as used in Table 1

Supplementary Table 3 – Evolutionary Distances (Myr) for the 12 species of Fig 1 & 2

Human 0 Bonobo 6.3 0 Macaque 29 29 0 Tarsier 65.2 65.2 65.2 0 Rat 92.3 92.3 92.3 92.3 0 Mouse 92.3 92.3 92.3 92.3 25.4 0 Guinea Pig 92.3 92.3 92.3 92.3 77.9 77.9 0 Hamster 92.3 92.3 92.3 92.3 43.9 43.9 77.9 0 Cow 94.2 94.2 94.2 94.2 94.2 94.2 94.2 94.2 0 Brandts Bat 94.2 94.2 94.2 94.2 94.2 94.2 94.2 94.2 81.6 0 Minke Whale 94.2 94.2 94.2 94.2 94.2 94.2 94.2 94.2 56 81.6 0 Opossum 162.6 162.6 162.6 162.6 162.6 162.6 162.6 162.6 162.6 162.6 162.6 0

Evolutionary distances were obtained from each pair of species using timetree.org.

A MyHC-6 α−Cardiac

100 Head Tail 98

96

94

92 - Minke Whale 90

MyHC-8 Perinatal 100

98

96

94

92

90

Sequence Identity (%) Identity Sequence 88

MyHC-10 Non-muscle B 100

98

96

94

92

90

88

86 0 50 100 150 1E-3 0.01 0.1 1 10 100 1000 Evol Dist (Myr) Mass (kg)

B MyHC-1 Skeletal 2x/d

100 Head Tail

98

96

94 - Golden Hamster - Minke Whale 92

MyHC-2 Skeletal 2a

100

98

96

94 - Golden Hamster - Tarsier

Sequence Identity (%) Identity Sequence 92

MyHC-4 Skeletal 2b

100

98

96

94 - Golden Hamster - Minke Whale 92 0 50 100 150 1E-3 0.01 0.1 1 10 100 1000 Evol Dist (Myr) Mass (kg)

C MyHC-11 Smooth Muscle

100 Head - Brandt's Bat Tail - Golden Hamster - Tarsier 98 - Bonobo

96

94

92

MyHC-13 Extraocular 100

96

92

88

84

Sequence Identity (%) 80 - Minke Whale

76

MyHC-7B/14 Slow Tonic

100

98

96

94

- Golden Hamster 92 - Opossum

90 0 50 100 150 1E-3 0.01 0.1 1 10 100 1000 Evolutionary Distance (Myr) Mass (kg)

Supplementary Figure 1. Evolutionary separation (right graph) and mass (left graph) of each pair compared to sequence divergence for nine common myosin II isoforms. The same set of twelve was used as in Figure 1 & 2 of the main paper. In some cases the full myosin sequences could not be located. Missing species are listed in each figure, in 4 cases 2 species were missing, in two cases the Minke whale was missing and in only for the smooth muscle myosin were 4 species absent. The regression line is drawn through the data and the slopes (SE) are shown in Figures 1 and 2 of the main paper.

Fig S2. Relationship between species mass, muscle shortening velocity and ADP release. A) The maximum shortening velocity of a muscle fibre expressing β-cardiac myosin and the mass of the species. Data in A replotted from Pellegrino et al (2003) J Physiol. 546, 677-689 based on Vo = d/τ, where Vo is the measured maximum shortening velocity, d is the distant over which the myosin cross-bridge remains strongly bound to actin and τ is the lifetime of the cross-bridge attachment. B) The correlation between the life-time of a cross-bridge predicted from the measured maximum shortening velocity in a muscle fibre (from A) and the measured lifetime of the A.M.ADP state. Data from Bloemink et al 2007 except human myosin which is from Deacon et al 2012. Based on τ = 1/kADP where kADP is the measured rate constant for ADP release and limits the rate of cross-bridge detachment.