Coming up for air

01/06/2015 |

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
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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
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What the fish have to say about how we found a voice

07/08/2014 |

A lone singer waits for darkness. 

Dusk falls.  As the waves push and pull at the sand with a steady rhythm, he revs up his vocal muscles for this, his love song. 

He begins to hum.  His baritone burr becomes louder and louder, booming across the bay.  After a few minutes, another voice joins in, slightly off pitch. 

They sing for over an hour.  Local residents head indoors, slamming windows to block out the noise.

The male plainfin midshipman fish has evolved to sing; not for ‘fun’ but to attract females to lay their eggs in his rocky burrow.  The call advertises his suitability to safeguard first the eggs and later the juvenile fry.  We usually associate parental care with mammals and birds.  For these territorial nesting fish, protection improves the survival of young at their most vulnerable life stage, which confers a considerable selectable advantage.

Sneaker male fish ‘cuckold’ the parental males. A cuckold is a man with an unfaithful wife, resulting in him bringing up someone else’s offspring. This term comes from the common cuckoo (Cuculus canorus), brood parasites which substitute their eggs into the nests of other birds. Their eggshell patterns match that of their smaller songbird host, so the surrogate parents (here a reed warbler, Acrocephalus scirpaceus) accept and rear the cuckoo’s outsized offspring (Image: Wikimedia Commons)

Sneaker male fish ‘cuckold’ the parental males. A cuckold is a man with an unfaithful wife, resulting in him bringing up someone else’s offspring. This term comes from the common cuckoo (Cuculus canorus), brood pa... morerasites which substitute their eggs into the nests of other birds. Their eggshell patterns match that of their smaller songbird host, so the surrogate parents (here a reed warbler, Acrocephalus scirpaceus) accept and rear the cuckoo’s outsized offspring (Image: Wikimedia Commons)

However these male fish come in two forms.  These other males are smaller, look like females, and like females they don’t sing.  When a real female is present they enter the nest and release sperm in the hope of fertilising some of the eggs.  Extreme competition for nest sites and breeding partners is thought to have selected for the evolution of these ‘sneaker’ males.  Male ‘cross-dressing’ cuckolds have been found in other animal species with extreme between-male competition for mates, some cuttlefish, lizards and dung beetles.

Singing male midshipman fish develop larger and more complex networks of vocal neurons in the brain than non-singers.  These networks, together with others that control the sense of hearing,  become more sensitive when the levels of sex hormones rise in the fish’ body.  These chemicals peak during the spawning season, prompting the males to sing and making the females more responsive.

In some ways the fish brain is a simpler version of our own, and other tetrapods.  Studying differences between the brains of these singing and non-singing male fish shows us how mate selection may have first prompted our ancestors to evolve a voice.

How does the male midshipman fish make his song?

The plainfin midshipman is one of several species of vocal fish that nest in the intertidal zone, creating a linear ‘lek’ along the coast.  Singing males hum by contracting a pair of sonic muscles attached to the swim bladder.  This pressurised air sac, used for buoyancy, shares developmental origins with our lungs  and helps the fish amplify his own voice.  Fast, synchronised contractions of the sonic muscles vibrate this ‘stiff-walled balloon’, generating sounds.

Skeletal muscles appear to have ‘stripes’ of fibres when seen under the microscope. This transmission electron microscope image shows human skeletal muscle fibres close up. The banding patterns visible here results from overlapping strands of actin and myosin proteins. Where the actin fibres overlap, they show up as the dark lines under the electron beam, known as Z lines. In plainfin midshipman singing males, the sonic muscle actin fibres overlap more, giving these fibres their unusually high tensile strength, and making the Z lines unusually wide and pronounced (Image: Wikimedia Commons)

Skeletal muscles appear to have ‘stripes’ of fibres when seen under the microscope. This transmission electron microscope image shows human skeletal muscle fibres close up. The banding patterns visible here results ... morefrom overlapping strands of actin and myosin proteins. Where the actin fibres overlap, they show up as the dark lines under the electron beam, known as Z lines. In plainfin midshipman singing males, the sonic muscle actin fibres overlap more, giving these fibres their unusually high tensile strength, and making the Z lines unusually wide and pronounced (Image: Wikimedia Commons)

All midshipman fish have sonic muscles.  In singing males these muscles are six times larger than in females and ‘sneaker’ males.  The singer’s muscle fibres are larger, four times as numerous, and surrounded by numerous mitochondria; the cell’s ‘power generators’.  Only these powerful muscles and a steady energy supply can sustain their hour-long mating call.

What inspires him to sing?

Singing males call only during the spawning season, and only at night.  The hormone melatonin, produced by the pineal gland, regulates this and other daily (circadian) and seasonal rhythms in the physiology and behaviour of vertebrates.  Longer hours of daylight in the spring lowers melatonin production, allowing the higher brain centres to release neurotransmitters.  These small protein signals trigger the production of sex hormones, which initiate nest building and singing behaviour in midshipman parental males.

A male and female Superb Fairy wren (Malurus cyaneus) from Western Australia. These birds pair-bond to raise their brood, although females often mate covertly with other males (cuckoldry). Male fairy wrens have unusually large testes (and hence high testosterone levels) for their body size, compared with similarly sized monogamous birds. This pattern is seen in other vertebrates where females mate with several males. Producing more sperm (by having larger testes) significantly affects their chances of breeding success through better sperm competition. ‘Sneaker’ male midshipman fish also have large testes relative to their body size; their limited opportunities to fertilise a female’s eggs means that if they are to succeed, their sperm must be highly competitive (Image: Wikimedia Commons)

A male and female Superb Fairy wren (Malurus cyaneus) from Western Australia. These birds pair-bond to raise their brood, although females often mate covertly with other males (cuckoldry). Male fairy wrens have unusuall... morey large testes (and hence high testosterone levels) for their body size, compared with similarly sized monogamous birds. This pattern is seen in other vertebrates where females mate with several males. Producing more sperm (by having larger testes) significantly affects their chances of breeding success through better sperm competition. ‘Sneaker’ male midshipman fish also have large testes relative to their body size; their limited opportunities to fertilise a female’s eggs means that if they are to succeed, their sperm must be highly competitive (Image: Wikimedia Commons)

Both singing and ‘sneaker’ males produce the male hormone testosterone.  However singers also produce a related chemical, 11-ketotestosterone, which enhances the performance of the vocal brain’s neural networks, and increases the growth of their sonic muscles.

The larger bodies of these singing males means they take longer to reach reproductive size, but potentially can mate with more females.  Sneaker males have the advantage of maturing quickly but the trade-off is that their reproductive success is uncertain.

How is the fish’s brain seasonally rewired for sound?

In singing males, seasonally high levels of 11-ketotestosterone make the vocal parts of the brain more responsive, prompting them to initiate their humming calls.  These brain regions contain ‘receptors’; that is protein ‘signal receivers’ that recognise the hormonal messages.  As the hormone binds, the receptor  changes shape into an active form and in turn modifies the genes which are employed by the vocal neurons to change their function.

A computer generated image of the human androgen receptor protein (coloured spirals) binding to a molecule of testosterone (in white). These signal decoding proteins bind testosterone, and become able to bind to short target sequences in the DNA. This affects which genes are being copied by the cell into RNA and used to build new proteins. More testosterone makes the fish’s nerve cells more sensitive to signals from other cells, triggering them to ‘fire’ more readily (Image: Wikimedia Commons)

A computer generated image of the human androgen receptor protein (coloured spirals) binding to a molecule of testosterone (in white). These signal decoding proteins bind testosterone, and become able to bind to short t... morearget sequences in the DNA. This affects which genes are being copied by the cell into RNA and used to build new proteins. More testosterone makes the fish’s nerve cells more sensitive to signals from other cells, triggering them to ‘fire’ more readily (Image: Wikimedia Commons)

In the part of the female fish’ ear that is the functional equivalent of our cochlea (the human hearing organ), oestrogen hormones are ‘seen’ by receptor proteins in a similar way. This renders her hearing more sensitive within the specific vocal range of the male’s droning call, enabling her to pick up its subtle nuances and high harmonics.

High oestrogen levels are also linked to better hearing in frogs and humans.

Text copyright © 2015 Mags Leighton. All rights reserved.

References
Arch, V.S. and Narins, P.M. (2009)  Sexual hearing: the influence of sex hormones on acoustic communication in frogs.  Hearing Research 252, 15-20.
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