How mouse-deer turned into whales – exploring evolution

What exactly is evolution? The broadest definition says that it is no more and no less than the heritable change in populations of organisms over time. But what is this change exactly, how does it come to be and what are the forces that drive it? As discussed in the previous post, the Theory of Evolution has been rewritten, expanded and corrected many times. Charles Darwin formulated the concept of natural selection in his widely celebrated book On the Origin of Species, but before him, others had come up with different mechanisms of evolution, and after him, many more discovered additional forces that made this process much more complex than Darwin had imagined. When biologists nowadays speak of evolution, they mean much more than natural selection, yet even that term is often misinterpreted. Evolution is a process driven by many different forces, some better understood than others, and is foremost a blind change of the natural world through time, that can be found embedded in its genetics.

To explain the different abstract concepts and mechanisms that make up the totality of evolution, it is probably best to use an example that speaks to our imagination. One of the most baffling cases of evolution can be found in the history of whales. Cetaceans - the scientific group that encompasses whales, dolphins and porpoises - share a similar appearance to their fellow, much more ancient neighbours of the sea - fish: they have pectoral fins, a strong hind tail and a dorsal fin that facilitates movement through water. Yet, they descend from a completely different branch of animals, and have roamed the oceans for a much briefer time[1]. After all, whales are mammals – and this can still be appreciated in much of their biology and anatomy: they have lungs and need to re-emerge to breathe the air, contrary to fish, who use gills to take up oxygen from water. They have no scales, and they are characterised by the one hallmark of the mammalian line: they wean their young and feed them milk. Indeed, they have adapted extremely well to their marine environment. This becomes all the more surprising when one takes into account that whales descend from hoofed, terrestrial mammals that still roamed this world 50 million years ago (about 15 million years after the extinction of the dinosaurs). Amazingly, although all terrestrial animals emerged from the water, cetaceans were some of the few[2] that returned to it and reversed the course of terrestrial evolution[3].

Some members of the infraorder Cetacea by Justin Hofman

Who were these mysterious land-dwelling ancestors? It has been widely accepted that cetaceans’ closest relatives are the artiodactyls, a group that comprises deer, antelopes, giraffes, pigs, camels and bovids. It is maybe not very surprising that within the artiodactyls, the semi-aquatic, yet terrestrial hippopotamus is whales' closest living cousin. One could intuitively assume that this is the intermediate form between the two groups and that whales descended from a primitive species of hippopotamus. This scenario was however invalidated by the discovery that hippos only emerged 15 million years ago and are therefore a much younger group than cetaceans.

It wasn’t until 2007 that a potential “missing link” was found that connected the artiodactyls to whales. In the Himalayan rock collection of the geologist A. Ranga Rao, scientists posthumously discovered the skull of an extinct, hoofed creature, which they named Indohyus. Through genetic and morphological comparisons, they showed that this tiny, strange land-dweller was indeed a sister species[4] of cetaceans and shared several traits both with them and with artiodactyls. Indohyus is in fact best compared to the extant group of chevrotains, which are miniature deer (also known as mouse-deer) that live in the forests of South East Asia and Africa. Indohyus’ heavy bone composition being similar to that of hippos suggests that it lived a semi-aquatic life. It has even been hypothesized, that Indohyus avoided predation by hiding over extensive periods of time under water, a strategy that is nowadays still being used by the water chevrotain, the only African species of living mouse-deer. Like modern artiodactyls, Indohyus was terrestrial and had four legs to walk on, yet several of its cranial and dental characteristics are only shared with cetaceans. This led to the general belief that Indohyus is an intermediary form in the transition of terrestrial ungulates to ocean-dwelling whales. Later forms of primitive whales, such as Pakicetus and Ambulocetus, start to show more and more adaptations to an aquatic lifestyle, and to resemble modern whales more closely.

Artistic reconstructions of Indohyus by Roman Uchytel and by Lucas Lima.

But how, and why did whales return to the sea and go through this extreme transformation? That part of the story is uncertain, but we know that each of the many different forces of evolution may, and most probably did, play a role in this process. The four fundamental forces of evolution are mutation, selection, genetic drift and gene flow. Additional to this, other forces have been described, but how large and universal a role they play in the shaping of life is still unclear[5]. Mutations[6] provide variation in a population: they slightly modify the genetic code of each individual and occur constantly and randomly when DNA is being copied and passed on to the next generation. This explains why individuals vary in their traits and characteristics: some are faster, others are stronger, some are of different colour, and others have a different size. Such differences do not always have a genetic basis – how tall you are is for example heavily influenced by your diet and other factors determined by experiences. Yet, for evolution to happen, trait differences need to be embedded in the genetic code so that they can be passed on to the next generation. This constant accumulation of genetic variation in a population is absolutely vital for all evolutionary forces to exert themselves.

Natural selection, Darwin’s most precious idea, still remains to be the best-known force of all. Under natural selection, whether an individual can survive until adulthood and pass on its unique set of genes to its offspring depends on how well adapted it is to its environment. For example, if a species is being predated, faster individuals might have a higher chance of survival, but if it has to break down trees to obtain food, the stronger individuals may have an advantage. Of course, biological traits are infinitely more intricate and complex than in these examples, but in the end, this myriad of tiny variations do add up to the best adapted, or “fittest” individual passing on its genes to the largest proportion of the next generation. If the environment remains stable over many generations, the traits that make individuals more fit to it will spread over the population until becoming a universal characteristic.

How does natural selection play into the story of our cetacean friends? For now, let’s assume that whales did indeed evolve from an Indohyus-like population of organisms, as has been proposed. Studies on Indohyus fossils suggested that, although it was already living a semi-aquatic life, it was in truth the change from terrestrial to aquatic prey that brought this omnivorous mouse-deer on the evolutionary path that led back to a life in the ocean and to the shaping of modern whales. Natural selection most probably played a large role in this: Indohyus might have lived in an environment where for some reason, terrestrial prey was less nutritional or harder to obtain compared to aquatic prey – maybe it was sparse, maybe the competition on land was more elevated, or maybe it was tougher to hunt down. If, by chance, an individual Indohyus started to feed on aquatic prey due to genetic changes, they would’ve been more successful and would’ve passed this new trait on to a large proportion of the next generation. This could then have led to a cascade of selective processes that caused at least part of the Indohyus population to specialize in an aquatic environment: every individual with a slightly better adapted body to feeding and eventually living in a marine habitat would contribute more to the next generation through the process of natural selection. Thus, Indohyus’ legs turned into fins, its skin lost its fur, its body started to accumulate blubber, until over the course of millions of years, it had become an unrecognisable marine creature that was excellent at moving in the water and catching fish – a new species altogether.

Phylogeny of ancient and modern whales: Cetacea and Artiodactyla split about 50 million years ago. Indohyus - still classified as Artiodactyl - forms the missing link between both groups. All subsequent forms of extinct whales are classified as Cetacea. As shown in the tree, none of the species of ancient whales are direct ancestors of each other - the tree merely shows their evolutionary relationships. Only two time points are indicated: the split of Artiodactyla and Cetacea and the split between toothed and baleen whales. Since it is not clear yet when exactly the different species of ancient whales arose and ceased to exist, I decided not to date the entire tree. Fossil dates are available, but are of course not an absolute indication of the life span of each individual species. The full tree has been composed by me, individual images are of various artists.

Interestingly, Charles Darwin himself already reflected in On the Origin of Species how such magnificent yet strange creatures as whales could have arisen through natural selection. Since in his time it was completely unknown from which land mammal cetaceans had descended, he suggested that they could’ve evolved from bears, since explorers had seen these swim for hours trying to catch prey in the water.

The course of evolution is not only determined by the environment and the individuals which are best adapted to it, but also by sheer chance. Such random processes are all bundled under the term genetic drift. An important consideration is that not all traits necessarily affect the fitness of an individual. Whether such “neutral” traits remain in the population, go to extinction or become fixed[7] is randomly determined based on pure chance. Yet, they are just as much part of a species’ set of characteristics as selectively evolving traits are and could even become selective themselves if the environment changes. Therefore, neutral traits also form an important role in shaping a species and its evolutionary course. In the case of whale evolution, we could wonder how much of a modern whales’ appearance was determined by natural selection improving Indohyus’ adeptness to a marine habitat, and how many traits are there merely by chance. A good example is the otherworldly size of baleen whales: these creatures feed on minuscule plankton, so why are they so large? Maybe natural selection pushed for a bigger size to prevent predation, but it might also be that neutral evolution pulled baleen whales towards the higher side of the size spectrum out of coincidence, since weight plays less of a role in water and plankton is available in magnificent quantities. We don’t have the answer.

The question of how great a role natural selection has played in the shaping of the entire Tree of Life compared to neutral evolution has been central since the early days of Evolutionary Biology and is still heavily debated and unresolved. On the other hand, neutral and selective regions of the genome can interact with one another – a phenomenon called genetic hitchhiking: genes that are under natural selection, can help the spread of neutral regions that lie physically close to them through the population. Hence, we can without a doubt be certain that the history of whales has also been written, in large or in small part, by neutral processes.

An extreme example of genetic drift that intensely shapes a species’ evolution is the population bottleneck. In a bottleneck, the population size reduces significantly in a short period of time due to a random environmental event, such as a volcanic eruption, an extreme drought, or the introduction of a highly competitive predator (for example, Homo sapiens). The result of the bottleneck is that a random set of individuals will survive. This will suddenly change the pool of genetic variation that is available for natural selection and other forces to act on. There are many examples of bottlenecks in nature’s history, and it is possible that also cetaceans went through one or several during their early history. In fact, whales went through a bottleneck in recent centuries because of our excessive hunting and are now slowly recovering. Bottlenecks have negative consequences for a species: the reduced genetic diversity often leads to inbreeding and the emergence of "unfit" traits such as genetically inherited illnesses. Moreover, a population with decreased genetic variation will overcome change with more difficulty. For example, if the oceans suddenly warm up, changing their currents and food resources, our whales of today will have a much harder time adapting to it quickly, since they have a reduced repertoire of varying traits at their disposal. This goes to show how important our understanding of evolutionary processes is to protect and conserve vulnerable, precious species such as our magnificent giants of the sea.

An analogy of the population bottleneck: each individual in a population represents a marble inside a bottle. The different colours of marbles represent the genetic diversity in the population. When a bottleneck occurs due to a catastrophic event that leads to a severe reduction in population size, only a couple of individuals survive, which leads to a general loss of genetic diversity in the population, as is shown here by the pouring of a couple of marbles into a glass. Image from pathwayz.org.

Last but not least, evolution is also being shaped by the process of gene flow, where different populations hybridise and exchange genes. This part of the evolutionary machine is still under intense examination by scientists who are desperate to unravel its intricate and mysterious ways of working. Isolated populations will inevitably diverge over time due to genetic drift, even if they live in a similar environment. Whether gene flow prevents or stimulates the isolation of populations is unclear. On one hand, new trait variants coming from a different population expand the gene pool, and the possibility exists that some of these variants even increase the fitness of the population to its own environment. Think for example about our modern whales who find themselves in an evolutionarily tricky situation due to the bottleneck they recently went through. The reduced genetic variation in their populations could be expanded through intermixing with other populations, which would in turn increase their chances of overcoming future threats as climate change. This form of adaptive gene flow would also prevent populations from drifting apart, since they share, at least partially, the same gene pool.

On the other hand, when two populations have already become considerably adapted to different environments, there is a high probability of the new variants being less adaptive and even deleterious ("unfit"). Selection pressures would then lead to the rise of a barrier that prevents such interbreeding from happening, for example by making females choose males only from their own population[8]. To give an example, if a population of orca which has adapted to hunt and feed on other marine mammals in cold water mixes with a population that is tuned to feed on shoals of fish in higher temperatures, it is probable that the hybrid offspring of these two populations would be neither well adapted to hunt fish nor mammals and survive in cold nor temperate waters. Since this would then lead to the hybrids having a lower fitness and survival rate overall, females choosing males from their own population are rewarded with more successful offspring. Such mechanisms stimulate the isolation of two populations, which will inevitably go down separate paths of evolution. Therefore, there is a contradictory line of thought that gene flow can both increase and decrease the fitness of a population and push for barriers between populations to both form and break down. It seems that the effect gene flow will have on populations depends tremendously on the extent to which the populations are isolated from each other and have already diverged.

Ambulocetus natans, another species of early whale whose fossils have been found in Pakistan. Although it was first thought that Ambulocetus could still walk, more recent studies suggest it being fully aquatic. Impression by Roman Uchytel.

There is no way of being sure whether gene flow played a large role in the evolution of whales, and how it did so. What we do know is that, at a certain point in history, some Indohyus-like organisms stopped interbreeding with their terrestrial relatives and undertook their own path of evolution into the depths of the ocean. This led to their isolation from other hoofed mammals that evolved in their own way to become camels, giraffes and wildebeests. It may have been that the early stages of transition to an aquatic habitat were slowed down because Indohyus still interbred with relatives which were not evolving in that direction. On the other hand, it could also be possible that Indohyus became physically isolated from its relatives for a long period of time, and diverged so much that mating became impossible later on. All we know for certain, is that at some point, the branch of Indohyus that evolved into whales stopped interbreeding extensively with its non-aquatic branch, so that a new species formed.

Although the list of evolutionary forces is longer and more complex than displayed here, the fundamental and best-known forces that underlie the genetic change in populations over time have now been laid out here one by one. Whales, dolphins and porpoises, such as any other animal, plant, fungus or microbe, have roamed and still roam this world because of an endlessly changing interaction of these processes. Over millions of years, the earth formed and changed its geography and environment through inner and outer forces: the movement of tectonic plates, the position of the sun and the moon, the composition of the atmosphere, and many more. At some point, life came to be and immediately started to diverge according to the earths varying environments over an endless stretch of time. Countless forms unimaginable to us reigned its thin surface, and then vanished into newer forms, sometimes tremendously fast, other times excruciatingly slowly. The earth saw explosions of flora and fauna when its conditions allowed it, followed by mass extinctions when they changed too suddenly. At some point, the world’s biodiversity incorporated the hominids and reached, in great part due to our own (often worrying) talent of shaping our environment, the state that we witness today. But we are no different from any other branch in the tree of life: we came from other life forms, and just like them arose from a very complicated chain of interactions between mutation, natural selection, genetic drift, gene flow and more, which eventually will also lead to our disappearance into new life forms, or into the layers of the earth. Life’s history is like a symphony of rich music, with its piano’s and crescendo’s, its solo’s and diminuendo’s, each and every note obeying the blind, magnificent conductor that is evolution.

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Footnotes:

[1] Such occurrence of similar traits in non-related lineages is called convergent evolution.

[2] Pinnipeds, that is to say seals, sea lions and walruses, also returned to the sea. They branch off from carnivorous mammals such as wolves, bears and weasles.

[3] As a reminder of whales’ terrestrial ancestors, one can still find remnants of once useful hind legs in the skeleton of some contemporary whales.

[4] Sister species are a pair of most closely related species, since they evolved from an evolutionary split and share an ancestor not shared by any other species.

[5] One of these would be the “selfish elements” – genetic regions which are inherited by more individuals than the laws of heredity would predict.

[6] Mutation often refers to single-letter changes in our DNA, but there are many other sources of variation that need to be included in this term, such as transposable elements, chromosomal rearrangements and recombination.

[7] A fixed trait is shared by all individuals of a population – there is no longer any variation.

[8] This form of selection, where not the environment, but potential mates select which individuals can pass on their genes, is called sexual selection and was also discussed by Darwin.

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For further reading/watching:

Original paper on the discovery of Indohyus as a missing link:

Thewissen, J. G., Cooper, L. N., Clementz, M. T., Bajpai, S., & Tiwari, B. N. (2007). Whales originated from aquatic artiodactyls in the Eocene epoch of India. Nature, 450(7173), 1190.

A review on early whale evolution and the cetacean fossil record:

Bajpai, S., Thewissen, J. G. M., & Sahni, A. (2009). The origin and early evolution of whales: macroevolution documented on the Indian Subcontinent. Journal of biosciences, 34(5), 673.

A (somewhat hilarious) video on the under-water hiding strategy of the water chevrotain:

https://www.youtube.com/watch?v=13GQbT2ljxs

A classic, and a good introduction to the process of evolution:

Dawkins, Richard (1976). The Selfish Gene. Oxford: Oxford University Press.

Another general introduction to Evolutionary Biology:

Zimmer, Carl (2001). Evolution: The Triumph of an Idea. Introduction by Stephen Jay Gould; foreword by Richard Hutton (1st ed.). New York: HarperCollins.