Coming up for air

Within a few hours of the naval sonar drill, reports arrived of stranded beaked whales appearing over many kilometres along the coast.  These animals showed signs of decompression sickness, also known as ‘the bends’.

Post-mortems on these animals revealed gas and fat bubbles in their bones and tissues.


The deeper you dive, the more the pressure forces nitrogen and oxygen from your lungs to dissolve into your body tissues.  If you then surface too quickly, these gases can come out of solution and form bubbles in your blood.  These can block smaller blood capillaries, cutting off the oxygen supply to the affected tissues.  Decompression sickness is a recurrent risk amongst scuba-divers who breathe compressed air, and breath-holding ‘free-divers’ who make too many consecutive dives.

We have a diving reflex like other mammals.  As the water hits our face, our heart slows and muscles under the skin contract, shunting blood into the centre of our body.  Water pressure increases by 1 Atmosphere for every 10m depth.  At 2 Atmospheres, the air in our lungs is half its original volume.  By 50 metres (5 Atmospheres), gaseous oxygen and nitrogen dissolves into our body tissues, and fluid floods into our lungs.  The human free-diving depth record is 214 metres (Image: Wikimedia Commons)

We have a diving reflex like other mammals. As the water hits our face, our heart slows and muscles under the skin contract, shunting blood into the centre of our body. Water pressure increases by 1 Atmosphere for every... more 10m depth. At 2 Atmospheres, the air in our lungs is half its original volume. By 50 metres (5 Atmospheres), gaseous oxygen and nitrogen dissolves into our body tissues, and fluid floods into our lungs. The human free-diving depth record is 214 metres (Image: Wikimedia Commons)

In contrast, beaked whales routinely hunt for an hour below 1000m, using echolocation.  These ‘extreme divers’ do not normally experience decompression sickness, although fossils from early in their evolutionary history show that they were not immune to these problems.  X-rays of the fossilised bones of more primitive whales show regions where bubbles formed inside a capillary, damaging the bone tissue and leaving a tell-tale signature.

Whale embryos initially develop rear limb buds, like land mammals.  These structures are reabsorbed back into the body later in development. The fossil record, along with DNA studies, reveal that whales’ closest living relatives are cows and hippos, which share their same four-legged (tetrapod), hoofed, land-dwelling ancestors.

Dolphin embryo (Image: Wikimedia Commons)

The hind limbs of this Spotted Dolphin embryo (Stenella frontalis) are visible as small bumps (limb buds) near the base of the tail.  (Image: Wikimedia Commons)

This raises some puzzling questions:

– Why did whales’ ancestors take to the water after 300 million years on land?

– Why didn’t they re-evolve gills?

– How can they dive for so long without getting ‘the bends’?

Why did whales’ air breathing ancestors take to the water?

These North Ronaldsay sheep are descended from an Orkney population farmed here since Neolithic times.  They graze along the shoreline, feeding almost exclusively on seaweed.  Their rumen stomachs have an adapted bacterial population which enables them to digest marine algae (Image: Wikimedia Commons)

These North Ronaldsay sheep are descended from an Orkney population farmed here since Neolithic times. They graze along the shoreline, feeding almost exclusively on seaweed. Their rumen stomachs have an adapted bacteria... morel population which enables them to digest marine algae (Image: Wikimedia Commons)

The land-dwelling ancestors of whales may have first waded into the sea to escape from predators on land.  Shallow coastal areas offered a relatively safe haven with little competition for the new food resources available in or near the water.  This initial stage would have enabled these semi-aquatic ancestors of modern whales to adapt their digestive systems to a marine food source.

Fossils from the early Eocene (52Ma) show a succession of increasingly aquatic forms.  From crocodile-like and otter -like amphibious hunters, developmental changes remodelled their breathing, senses, kidney function and limbs to survive better in water.  By 40Ma, these early whales had flippers, a fluked tail, and could mate, birth and suckle their young without leaving the water.

At the Eocene-Oligocene boundary (around 36Ma), movement of the continental plates opened up the deep waters of the circum-Antarctic ocean.  This offered new ecological roles for the deeper-diving whales.  Many new whale species appeared, including ancestors of the filter-feeding baleen whales and toothed whales that hunt in deep waters using echolocation.

Why didn’t whales re-evolve gills?

A sperm whale (Physeter macrocephalus) begins a dive; Gulf of Mexico.  Adaptations for cold, deep waters include insulating blubber, lungs designed to collapse under pressure, and locomotion.  The fluked tail is a super-efficient ‘caudal oscillator’; both the up and down strokes generate lift, like a birds’ wing.  These and other whale and seal species dive deep both to forage and to escape from killer whale (Orcinus orca) attacks (Image: Wikimedia Commons)

A sperm whale (Physeter macrocephalus) begins a dive; Gulf of Mexico. Adaptations for cold, deep waters include insulating blubber, lungs designed to collapse under pressure, and locomotion. The fluked tail is a super-e... morefficient ‘caudal oscillator’; both the up and down strokes generate lift, like a birds’ wing. These and other whale and seal species dive deep both to forage and to escape from killer whale (Orcinus orca) attacks (Image: Wikimedia Commons)

The ability to breathe underwater like fish seems at first like a requirement for life in the sea.  However despite their lack of gills, whales and dolphins are highly effective predators in both shallow and deep water.

Modern whales’ warm bodies enable their fast reflexes for hunting.  Whilst swordfish and tuna have some warm muscles, most of their tissues are at sea water temperature.  Were their whole bodies warm, the heat loss from their gills would be energetically too costly.

Fish gills develop from the ‘branchial arches’; bulging structures in the early vertebrate embryo.  These same tissue bulges give rise to the lower jaw, the middle ear, hyoid bone and larynx in the throat of humans and other mammals.  For whales and other mammals to form gills would require that they develop new embryonic structures; this would render redundant the lungs with their vast area of vascular tissue.

Breathing air enables whales to use vocal signals to coordinate their social groups and attract mates.  Like land mammals, the baleen whales make vocal calls by passing a controlled air flow through the larynx.  Echolocation, the alternative means of producing sound used by dolphins and other toothed whales, also requires air.  Their ‘sonic lips’ generate calls in an air-filled nasal passage.  Whilst many fish make sounds, their vocal abilities are simple and limited.

How do they dive for so long without getting ‘the bends’?

This diagram shows how myoglobin forms ‘alpha-helical’ spirals around a ‘haem’ co-factor.  Haem’s ring-structure holds an iron atom, carrying an electrostatic charge.  This attracts and holds an oxygen molecule (red spheres).  As carbon dioxide builds up it dissolves to form carbonic acid.  This change of pH, alters the electrostatic balance, prompting myoglobin to release its oxygen.  The myoglobin protein’s high positive charge also steadies the pH when cells break down sugars without oxygen and produce lactic acid (Image: Wikimedia Commons)

This diagram shows how myoglobin forms ‘alpha-helical’ spirals around a ‘haem’ co-factor. Haem’s ring-structure holds an iron atom, carrying an electrostatic charge. This attracts and holds an oxygen molecule ... more(red spheres). As carbon dioxide builds up it dissolves to form carbonic acid. This change of pH, alters the electrostatic balance, prompting myoglobin to release its oxygen. The myoglobin protein’s high positive charge also steadies the pH when cells break down sugars without oxygen and produce lactic acid (Image: Wikimedia Commons)

All mammals store oxygen in their muscles using a protein called myoglobin.  Sustained activity during long foraging dives requires a lot of oxygen.  Deep divers have much higher muscle myoglobin concentrations than land mammals, giving them substantial oxygen reserves.

Modern diving mammals, and deep diving fish such as tuna, have also modified their myoglobin.  As early whales began to explore the deeper waters, selection resulted in better survival from individuals whose myoglobin carried a stronger positive electrostatic charge.   Like positive magnetic poles, these ‘supercharged’ molecules repel each other.  This keeps them in solution, allowing them to function at high tissue concentrations where most other proteins would clump together.

A supercharged form and high concentration of myoglobin makes it possible for deep diving mammals to return to the surface slowly after a prolonged dive.  This behaviour avoids decompression sickness.

However when beaked whales and other species encounter naval sonar at depth, this causes them to ‘panic’ and surface too quickly, inducing ‘the bends’.

Text copyright © 2015 Mags Leighton. All rights reserved.

References
Balasse M et al. (2006) ‘Stable isotope evidence (δ13C, δ18O) for winter feeding on seaweed by Neolithic sheep of Scotland’ Journal of Zoology 270(1); 170-176
Beatty B L & Rothschild B M (2008)  ‘Decompression syndrome and the evolution of deep diving physiology in the Cetacea’  Naturwissenchaft 95;793-801
Costa D P (2007) Diving physiology of marine vertebrates’ Encyclopedia of life sciences doi:10.1002/9780470015902.a0004230
Ferguson S H et al. (2012) ‘Prey items and predation behavior of killer whales (Orcinus orca) in Nunavut, Canada based on Inuit hunter interviews’  Aquatic Biosystems 8 (3); http://www.aquaticbiosystems.org/content/8/1/3
Gatesy J et al. (2013) ‘A phylogenetic blueprint for a modern whale’  Molecular Phylogenetics and Evolution’ 66:479-506
Mirceta S et al. (2013) ‘Evolution of mammalian diving capacity traced by myoglobin net surface charge’  Science 340;1234192
Nery M F et al. (2013) ‘Accelerated evolutionary rate of the myoglobin gene in long-diving whales’  Journal of Molecular Evolution 76;380-387
Noren S R et al. (2012) ‘Changes in partial pressures of respiratory gases during submerged voluntary breath hold across odontocetes; is body mass important?’  Journal of Comparative Physiology B 182;299-309
Orpin C G et al. (1985) ‘The rumen microbiology of seaweed digestion in Orkney sheep’  Journal of Microbiology 58(6); 585-596
Rothschild B M et al (2012) ‘Adaptations for marine habitat and the effect of Jurassic and Triassic predator pressure on development of decompression syndrome in ichthyosaurs’  Naturwissenchaften 99;443-448
Steeman M E et al. (2009) ‘Radiation of extant cetaceans driven by restructuring the oceans’  systematic biology 58;573-585
Thewissen J G M et al (2007) ‘Whales originated from aquatic artiodactyls in the eocene epoch of India’  Nature 450;1190-1195
Thewissen J G M et al (2006) ‘Developmental basis for hind-limb loss in dolphins and origin of the cetacean body plan’ Proceedings of the National Academy of Sciences USA 103(22); 8414–8418
Thewissen J G M and Sunil B (2001) ‘Whale origins as a poster child for macroevolution’  Bioscience 51(12);1037-1049
Tyack P L (2006) ‘Extreme diving of beaked whales’  Journal of Experimental Biology 209;4238-4253 Naturwissenchaften 99:443-448
Uhen M D (2010) ‘The origin(s) of whales’  Annual Review of Earth and Planetary Sciences 38;189-219
Uhen M D (2007) ‘Evolution of marine mammals; back to the sea after 300 million years’  The Anatomical Record 290;514-522
Williams T M (1999) ‘The evolution of cost efficient swimming in marine mammals; limits to energetic potimization’  Philosohical Transactions of the Royal Society of London series B  354;193-201

Making waves; how moving our arms as we talk signals our ‘inner fish’

The old Jewish Cemetery; Venice, 1790. 

Goethe loosens the earth from the skull, and holds it up to the sun. 

Turning the fractured bone back and forth, he gasps.  A series of marks appear inside the cavity, reminding him of the vertebrae.  He has looked at this pattern many times, but without seeing what lights up before him today. 

Here is the shadow of a blueprint; the ‘primal repeating units’ of animal bodies, from which their many variations form. 

Puzzled, Götze watches his master’s eyes shine with delight. 


Watch this baby babbling; her limbs move, often in time with her sounds.  the coupling of gestures and vocal calls are widespread amongst social vertebrates.  And the story began with fish.

Watch this baby babbling. The rhythmical arm and leg movements of human infants as they vocalise reveals some ancient neural wiring, inherited from our common vertebrate ancestors, and now shared with other modern vertebrates from elephants through reptiles, amphibians and birds to fish (Image: Wikimedia Commons)

Watch this baby babbling.The rhythmical arm and leg movements of human infants as they vocalise reveals some ancient neural wiring, inherited from our common vertebrate ancestors, and now shared with other modern verteb... morerates from elephants through reptiles, amphibians and birds to fish (Image: Wikimedia Commons)

The rhythm of our breath keeps us alive.  Conscious muscle movements are made through spinal nerve reflexes, but like our heart beats, the repeating sequences of muscle actions which fill and empty our lungs are outside our conscious awareness.

The movements behind repetitive activities like breathing are driven by rhythmic nerve impulses from ‘neural oscillators’.  These pattern-generating circuits, located in the central nervous system, are known as ‘Central Pattern Generators’.

To breathe, to speak and to swallow we use the same internal tube; that is our throat (the pharynx).  These activities are necessarily exclusive; consider what happens when a crumb ‘goes down the wrong way’.  Speech therefore needs to be coordinated with our breathing.

The male club-winged manakin (Machaeropterus deliciosus) from the cloud forests of Ecuador makes sounds by rapid wing vibrations.  This rhythmic movement is driven by the vertebrate vocal central pattern generators.  The line drawing (shown right), from Charles Darwin’s book The descent of man, shows how the male birds’ secondary flight feathers (top ) are modified for sound (the equivalent feathers from the female bird are shown in the bottom row).  Watch. (Images: Wikimedia Commons)

The male club-winged manakin (Machaeropterus deliciosus) from the cloud forests of Ecuador makes sounds by rapid wing vibrations. This rhythmic movement is driven by the vertebrate vocal central pattern generators. The ... moreline drawing (shown right), from Charles Darwin’s book The descent of man, shows how the male birds’ secondary flight feathers (top ) are modified for sound (the equivalent feathers from the female bird are shown in the bottom row). Watch. (Images: Wikimedia Commons)

We make vocal sounds by passing air through the larynx as we breathe out, at the same time as vibrating our vocal folds (vocal cords).  These actions involve coordinating a sequence of repetitive movements inside the throat with the repeating muscle actions that drive our breath.

Communicating with sound evolved long before animals emerged from the sea onto land and began to breathe air.  Many fish use pectoral fin movements as communication gestures; some also generate sounds by fin waving.

In species of vocal fish, the calls are coordinated with these pectoral fin signals.  Significantly, the muscles operating these social communication cues are controlled using the same neural oscillator ‘module’.

‘Central Pattern Generators’ are neural oscillators that generate a rhythmic output, used to control repeating muscle movements.  These ‘neural metronomes’ were first discovered in insects, and produce their steady pulse without any sensory stimulus.  In contrast, our other nerves operate on a ‘stimulus-response’ basis.

The predictable and repetitive movements we use for breathing, chewing and walking can speed up and slow down, but the sequence in which these muscles work (the oscillatory cycle) does not change. Oscillators are known ... morein mechanical, chemical and biological systems. This simple (undampened) oscillating spring can alter its speed, but the nature of the movement remains the same (Image: Wikimedia Commons)

 

Central Pattern Generators reveal what can be called our ‘deep homology’.  First discovered in insects, all vertebrates, including ourselves, have these ancient neural circuits.  They links vocal calls with gestures, and coordinate our ‘fins’ with our speech.

How do Central Pattern Generators work? 

We consciously control our limbs through spinal nerve reflex arcs.  In contrast, rhythmic movements controlling oscillating cycles are driven by Central Pattern Generators (CPGs).  These autonomous modules in the central nervous system produce a rhythmic output (like a neural ‘black box’).  CPG modules are comprised of a dense interconnected local network of neurons; a neural ‘node’.

These nodes are organised into three levels, each with a different function, and in each case, the parts of the circuit ‘higher’ in this organisation regulate the outputs of those below.

The vocal Central Pattern Generator used to produce basic signals for social communication, is organised in much the same way in fish, frogs, birds and mammals.  Like all Pattern Generator modules it has a hierarchical organisation.   i.pre-pacemaker cells set the duration of the output,  ii.pacemaker neurons set the frequency of the regular nerve impulse iii.Motor neurons transmit the pacemaker’s rhythmic output to the muscles (Image: Wikimedia Commons)

The vocal Central Pattern Generator used to produce basic signals for social communication, is organised in much the same way in fish, frogs, birds and mammals. Like all Pattern Generator modules it has a hierarchical o... morerganisation.i. pre-pacemaker cells set the duration of the output,ii. pacemaker neurons set the frequency of the regular nerve impulseiii. Motor neurons transmit the pacemaker’s rhythmic output to the muscles (Image: Wikimedia Commons)

In the developing embryo there are functional units, ‘segments’ which give rise to our vertebrae and their associated nerves and muscles.  The nerves from each of these ‘segments’ form our local sensory spinal reflexes and also the CPG modules.  As needed, higher brain centres trigger these ‘neural motors’ to produce their rhythmical nerve impulses and drive all of our rhythmical movements from walking to chewing.

CPGs controlling rhythmic movements of the tongue, throat and breathing (including the vocal neural oscillator module) are in the lower brainstem and neck.  The CPGs that drive the rhythm of our walking are low down in the spinal cord, in the thoracic and lumbar regions.

Why don’t we sound like fish? 

Vocal fish such as this Oyster toadfish (Opsanus tau) produce calls in one of two ‘output modes’.  This is controlled by testosterone, which reduces the threshold of nerve stimulus needed to initiate calls.  In ‘normal’ mode, these fish are able to sustain only slow rhythmic grunts.  ‘Mating mode’ speeds up these sounds into a buzzing drone. Mating calls are made only at night during the spawning season, when testosterone levels are high.   In this video clip the closely related plainfin midshipman fish (Porichthys notatus) demonstrates both call types (Image: Wikimedia Commons)

Vocal fish such as this Oyster toadfish (Opsanus tau) produce calls in one of two ‘output modes’. This is controlled by testosterone, which reduces the threshold of nerve stimulus needed to initiate calls. In ‘nor... moremal’ mode, these fish are able to sustain only slow rhythmic grunts. ‘Mating mode’ speeds up these sounds into a buzzing drone. Mating calls are made only at night during the spawning season, when testosterone levels are high.In this video clip the closely related plainfin midshipman fish (Porichthys notatus) demonstrates both call types (Image: Wikimedia Commons)

Toadfish vocalise with either a sequence of repetitive grunts during aggressive encounters or the prolonged drone of their mating call.  In both cases, each nerve impulse from the vocal pattern generator produces a single synchronised contraction in their sonic muscles; this muscle pair flexes the rigid walls of the swimbladder, producing a ‘grunt’.  This sound receives no further processing.  As a result, its tone is rather mechanical.

Our voice, like that of frogs, birds and mammals, also begins with this simple rhythmic sound pulse.  This initial sound is then processed into croaks, calls songs and speech.  Our neck  allows us to create resonant areas in the throat which amplify certain frequencies.  Pitch is affected by vocal fold (vocal cord) tension, and manipulation of our tongue and lips produces precisely articulated words.

Why is ‘talking with our hands’ still a part of our language?

This Siamese fighting fish (Betta splendens) uses rapid pectoral fin movements as a posturing signal during competitive displays with other males. Watch displaying fish in adjacent tanks using pectoral fins signals (Image: Wikimedia Commons)

This Siamese fighting fish (Betta splendens) uses rapid pectoral fin movements as a posturing signal during competitive displays with other males. Watch displaying fish in adjacent tanks using pectoral fins signals (Image: Wikimedia... more Commons)

Many vocal fish make synchronised gestures with their front (pectoral) fins during mating calls.  These motor nerve connections from our ancient common ancestor are retained in other vertebrates.

People blind from birth move their hands when they talk.  Our vocal Pattern Generator circuits connects with both our larynx and pectoral muscles, coordinating our speech with our ‘body language’.  We subconsciously move our hands as we communicate thanks to these rhythmic central circuits.  As in all other vertebrates, we have inherited these from (as Palaeontologist Neil Shubin puts it) our ancestral ‘inner fish’.

Text copyright © 2015 Mags Leighton. All rights reserved.

References
Aboitiz, F. (2012)  Gestures, vocalizations, and memory in language origins.  Frontiers in Evolutionary Neuroscience 4, e2.
Bass, A.H. and Chagnaud, B.P. (2012)  Shared developmental and evolutionary origins for neural basis of vocal-acoustic and pectoral-gestural signalling.  Proceedings of the National Academy of Sciences, USA 109 (Suppl.1), 10677-10684.
Bass, A.H. et al. (2008)  Evolutionary origins for social vocalization in a vertebrate hindbrain-spinal compartment.  Science 321, 417-421.
Bostwick, K.S. (2000) Display behaviors, mechanical sounds, and evolutionary relationships of the Club-winged Manakin (Machaeropterus deliciosus). Auk 117, 465-478.
Bostwick, K.S. et al. (2010)  Resonating feathers produce courtship song. Proceedings of the Royal Society, B 277, 835-841.
Chagnaud, B.P. et al. (2012)  Innovations in motoneuron synchrony drive rapid temporal modulations in vertebrate acoustic signalling.   Journal of Neurophysiology 107, 3528-3542.
Dick, A.S. et al. (2012)  Gesture in the developing brain.  Developmental Science 15, 165–180.
Ghazanfar, A.A. (2013) Multisensory vocal communication in primates and the evolution of rhythmic speech. Behavioral Ecology and Sociobiology 67, 1441-1448.
Goethe, J.W. (1820).  Zur Naturwissenschaften überhaupt, besonders zur Morphologie; cited (p. 7) in G.R. de Beer The Development of the Vertebrate Skull.  Clarendon (1937).
Guthrie, S. (1996)  Patterning the hindbrain.  Current Opinion in Neurobiology 6,41-48.
Hanneman, E. et al. (1988) Segmental pattern of development of the hindbrain and spinal cord of the zebrafish embryo. Development 103, 49-58.
Iverson, J.M. and Thelen, E. (1999)  Hand, mouth and brain: The dynamic emergence of speech and gesture.  Journal of Consciousness Studies 6, 19-40.
Kelley, D.B. and Bass, A.H. (2010)  Neurobiology of vocal communication: mechanisms for sensorimotor integration and vocal patterning. Current Opinion in Neurobiology 20,748-53.
Marder, E. and Bucher, D. (2001)  Central pattern generators and the control of rhythmic movements.  Current Biology 11, R986-R996.
Shubin, N (2008)  Your inner fish; a journey into the 3.5 Billion year history of the human body.  Penguin Books Ltd.
Shubin, N. et al. (2009)  Deep homology and the origins of evolutionary novelty.  Nature 457, 818-823.