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Home , Neobalaenidae

Genomic Evidence for Diving Behavior in the Pygmy

Mark S. Springer Department of Evolution, Ecology, and Organismal Biology University of California Riverside

Coauthors: John Gatesy, Phil Morin, Michael Berenbrink, Kevin Campbell, Matthew Collin, Taku Kishida, Gang Li, William Murphy

• Part of larger NSF project on cetacean genomics (“The Phylogeny and Evolution of : Resolution of Rapid Radiations and a Molecular Blueprint for Modern Whales, Dolphins, and ”) • Most samples from Southwest Fisheries • Target for sequence coverage: ~30-35X Illumina PIs/co-PIs: Collaborators: John Gatesy Michael Berenbrink Phil Morin Kevin Campbell Mark Springer Matthew Collin Christopher Emerling Jeffry Fasick Michael Hiller Nikolai Hecker Matthias Huelsmann Jeremy Johnson Takushi Kishida Gang Li Michael McGowen William Murphy Ji Won Oh Maksim Plikus Amy Van Cise Taxon Sampling (New Genomes + Publicly Available Genomes) Family Number of species in Number of sampled family species/individuals 4 3/5 Neobalaenidae 1 1/1 Eschrichidae 1 1/5 Balaenopteridae 9 8/14 Physeteridae 1 1/1 Kogiidae 2 2/3 Ziphiidae 22 15/17 Platanisdae 2 1/1 Lipodae 1 1/1 3 1/1 Pontoporiidae 1 1/2 Delphinidae 39 33/43 Monodondae 2 2/4 Phocoenidae 7 4/4 Totals 95 74/101 Caperea marginata ()

• Smallest mysticete and the only living member of the family Neobalaenidae

• Found in Southern Hemisphere

Phylogenetic Position of Neobalaenidae • Unequivocal based on molecular data

Gatesy et al. (2013) • Equivocal based on morphology

Biscon (2012)

Fordyce and Marx (2012) Vision: Rods and Cones

• Rods: scotopic vision

• Cones: photopic vision Visual Opsins in Vertebrates

SWS1 SWS2 RH2 RH1 LWS

500-501 355 416 467-505 548-558 1.0

0.8

0.6

0.4

0.2

0.0 400 500 600 700 Wavelength (nm) Visual Opsins

• Rods: RH1 • Cones: RH2, SWS1, SWS2, LWS

RH1 RH2 SWS2 SWS1 LWS Loss of Cone Opsins in

Figure from Jacobs (2013) Trichromatic Vision in Humans and Various Primates Cone monochromacy in a variety of mammals

Carnivora

Table from Cetacea Jacobs (2013)

Chiroptera

Primates

Rodena Are there also rod monochromats?

”…. absolutely cone-free retina which once were duplex, and have lost their cones, are known for a certainty to occur only in deep-sea fishes, the bats, and the armadillo. Some others probably have only rods...the hedge-hog, the guinea-pig, the whales and seals, most lemuroids and Aotus..." (Walls 1942)

”… the histological and chemical evidence suggest that vision in cetacea is based on only one retinal pigment, a rhodopsin." (McFarland 1971) Ziphius cavirostris (Schorr et al. 2014) Inactivation of Opsins in Cetacea

1

2

3 4

5

Meredith et al. (2013, PLoS Genetics) Examples of Frameshift Mutations in LWS Intact LWS and Blueshifted RH1 in Caperea

Meredith et al. (2013, PLoS Genetics) Meredith et al. (2013) Possible Significance of Blueshift in RH1

Light Penetraon in Open Water (Clear Day) Wavelength (nanometers) Pygmy Right Whale Versus Other Mysticetes

LWS Intact RH1 λmax

Pygmy right Yes 479 nm whale Other No 484-493 nm mysticetes

LWS is intact in the pygmy right whale, but is the cone phototransducon cascade intact? Opsins and Other Retinal Protein Genes

Emerling and Springer 2014, MPE Phototransduction Visual Cycle Cone Monochromatic Cetaceans Physeter macrocephalus mysticetus

LWS PDE6C CNGA3 LWS PDE6C CNGA3 LWS PDE6C CNGA3 GNAT2 GNAT2 GNAT2

SWS1 PDE6H CNGB3 SWS1 PDE6H CNGB3 SWS1 PDE6H CNGB3 GNB3 GNGT2 GNB3 GNGT2 GNB3 GNGT2

Balaenoptera physalus bonaerensis Balaenoptera acutorostrata

LWS PDE6C CNGA3 LWS PDE6C CNGA3 LWS PDE6C CNGA3 GNAT2 GNAT2 GNAT2

SWS1 PDE6H CNGB3 SWS1 PDE6H CNGB3 SWS1 PDE6H CNGB3 GNB3 GNGT2 GNB3 GNGT2 GNB3 GNGT2

Springer et al. (2016) What about the pygmy right whale?

Is there any evidence for ablation of the cone phototransduction pathway in this species?

Made use of gap-closed assembly for Caperea

Total bases 2234886559 Min sequence length 1000 Max sequence length 280268 Average sequence length 15245.00 Median sequence length 7945.50 N50 length 31075 N75 length 15891 N90 length 7473 N95 length 4323 As 29.67 % Ts 29.18 % Gs 20.51 % Cs 20.56 % (A + T)s 58.85 % (G + C)s 41.07 % Ns 0.08 %

Conclusion: The cone phototransduction cascade in inactivated in the pygmy right whale even though LWS is intact. What about myoglobin?

Molecular Aqualung: Key protein in muscle that shows evidence for increased net surface charge in elite mammalian divers

Mirceta et al. (2013) Pygmy Right Whale Myoglobin

Additional histidine at position 66 of mature protein

Parallel change with deep diving ziphiids

Surface charges:

Most mysticetes = 3.65 Pygmy right whale = 3.92 Minke whale: 3.94 = 4.15-4.24 Beaked whales = 4.80

Conclusions

• The pygmy right whale is a rod monochromat

• An inactivated cone phototransduction cascade, a blueshifted RH1, and an increased surface charge on myoglobin suggest enhanced diving capabilities in the pygmy right whale