Speciation – Science Sushi

Evolution: The Rise of Complexity

Let’s rewind time back about 3.5 billion years. Our beloved planet looks nothing like the lush home we know today – it is a turbulent place, still undergoing the process of formation. Land is a fluid concept, consisting of molten lava flows being created and destroyed by massive volcanoes. The air is thick with toxic gasses like methane and ammonia which spew from the eruptions. Over time, water vapor collects, creating our first weather events, though on this early Earth there is no such thing as a light drizzle. Boiling hot acid rain pours down on the barren land for millions of years, slowly forming bubbling oceans and seas. Yet in this unwelcoming, violent landscape, life begins.

The creatures which dared to arise are called cyanobacteria, or blue-green algae. They were the pioneers of photosynthesis, transforming the toxic atmosphere by producing oxygen and eventually paving the way for the plants and animals of today. But what is even more incredible is that they were the first to do something extraordinary – they were the first cells to join forces and create multicellular life.

It’s a big step for evolution, going from a single cell focused solely on its own survival to a multicellular organism where cells coordinate and work together. Creationists often cite this jump as evidence of God’s influence, because it seems impossible that creatures could make such a brazen leap unaided. But scientists have shown that multicellularity can arise in the lab, given strong enough selective pressure.

Just ask William Ratcliff and his colleagues at the University of Minnesota. In a PNAS paper published online this week, they show how multicellular yeast can arise in less than two months in the lab. To achieve this leap, they took brewer’s yeast – a common, single celled lab organism – and grew them in a liquid medium. Once a day, they gently spun the yeast in the culture, starting the next batch with whichever cells ended up at the bottom of the tube. Because the force of spinning pulls larger things down first, clumps of cells were more likely to be at the bottom than single ones, thus setting up a strong selective pressure for multicellularity.

Evolution of Snowflake Yeast — Images of the snowflake-like pattern that arose in all of the experimental cell cultures from Ratcliff et al. 2012

All of their cultures went from single cells to snowflake-like clumps in less than 60 days. “Although known transitions to complex multicellularity, with clearly differentiated cell types, occurred over millions of years, we have shown that the ?rst crucial steps in the transition from unicellularity to multicellularity can evolve remarkably quickly under appropriate selective conditions,” write the authors. These clumps weren’t just independent cells sticking together for the sake of it – they acted as rudimentary multicellular creatures. They were formed not by random cells attaching but by genetically identical cells not fully separating after division. Furthermore, there was division of labor between cells. As the groups reached a certain size, some cells underwent programmed cell death, providing places for daughter clumps to break from. Since individual cells acting as autonomous organisms would value their own survival, this intentional culling suggests that the cells acted instead in the interest of the group as a whole organism.

Given how easily multicellular creatures can arise in test tubes, it might then come as no surprise that multicellularity has arisen at least a dozen times in the history of life, independently in bacteria, plants and of course, animals, beginning the evolutionary tree that we sit atop today. Our evolutionary history is littered with leaps of complexity. While such intricacies might seem impossible, study after study has shown that even the most complex structures can arise through the meandering path of evolution. In Evolution’s Witness, Ivan Schwab explains how one of the most complex organs in our body, our eyes, evolved. Often touted by Intelligent Designers as ‘irreducibly complex’, eyes are highly intricate machines that require a number of parts working together to function. But not even the labyrinthine structures in the eye present an insurmountable barrier to evolution.

Our ability to see began to evolve long before animals radiated. Visual pigments, like retinal, are found in all animal lineages, and were first harnessed by prokaryotes to respond to changes in light more than 2.5 billion years ago. But the first complex eyes can be found about 540 million years ago, during a time of rapid diversification colloquially referred to as the Cambrian Explosion. It all began when comb jellies, sponges and jellyfish, along with clonal bacteria, were the first to group photoreceptive cells and create light-sensitive ‘eyespots’. These primitive visual centers could detect light intensity, but lacked the ability to define objects. That’s not to say, though, that eyespots aren’t important – eyespots are such an asset that they arose independently in at least 40 different lineages. But it was the other invertebrate lineages that would take the simple eyespot and turn it into something incredible.

According to Schwab, the transition from eyespot to eye is quite small. “Once an eyespot is established, the ability to recognize spatial characteristics – our eye definition – takes one of two mechanisms: invagination (a pit) or evagination (a bulge).” Those pits or bulges can then be focused with any clear material forming a lens (different lineages use a wide variety of molecules for their lenses). Add more pigments or more cells, and the vision becomes sharper. Each alteration is just a slight change from the one before, a minor improvement well within bounds of evolution’s toolkit, but over time these small adjustments led to intricate complexity.

Cambrian Arthropod Eyes — Fossilized compound eyes from Cambrian arthropods (Lee et al. 2011)

In the Cambrian, eyes were all the rage. Arthropods were visual trendsetters, creating compound eyes by using the latter approach, that of bulging, then combining many little bulges together. One of the era’s top predators, Anomalocaris, had over 16,000 lenses! So many creatures arose with eyes during the Cambrian that Andrew Parker, a visiting member of the Zoology Department at the University of Oxford, believes that the development of vision was the driver behind the evolutionary explosion. His ‘Light-Switch’ hypothesis postulates that vision opened the doors for animal innovation, allowing rapid diversification in modes and mechanisms for a wide set of ecological traits. Even if eyes didn’t spur the Cambrian explosion, their development certainly irrevocably altered the course of evolution.

Our eyes, as well as those of octopuses and fish, took a different approach than those of the arthropods, putting photo receptors into a pit, thus creating what is referred to as a camera-style eye. In the fossil record, eyes seem to emerge from eyeless predecessors rapidly, in less than 5 million years. But is it really possible that an eye like ours arose so suddenly? Yes, say biologists Dan-E. Nilsson and Susanne Pelger. They calculated a pessimistic guess as to how long it would take for small changes – just 1% improvements in length, depth, etc per generation – to turn a flat eyespot into an eye like our own. Their conclusion? It would only take about 400,000 years – a geological instant.

But how does complexity arise in the first place? How did cells get photoreceptors, or any of the first steps towards innovations such as vision? Well, complexity can arise a number of ways.

endosymbiosis_c_la_784 — An illustration of the endosymbiont hypothesis

Each and every one of our cells is a testament to the simplest way that complexity can arise: have one simple thing combine with a different one. The powerhouses of our cells, called mitochondria, are complex organelles that are thought to have arisen in a very simple way. Some time around 3 billion years ago, certain bacteria had figured out how to create energy using electrons from oxygen, thus becoming aerobic. Our ancient ancestors thought this was quite a neat trick, and, as single cells tend to do, they ate these much smaller energy-producing bacteria. But instead of digesting their meal, our ancestors allowed the bacteria to live inside them as an endosymbiont, and so the deal was struck: our ancestor provides the fuel for the chemical reactions that the bacteria perform, and the bacteria, in turn, produces ATP for both of them. Even today we can see evidence of this early agreement – mitochondria, unlike other organelles, have their own DNA, reproduce independently of the cell’s reproduction, and are enclosed in a double membrane (the bacterium’s original membrane and the membrane capsule used by our ancestor to engulf it). Over time the mitochondria lost other parts of their biology they didn’t need, like the ability to move around, blending into their new home as if they never lived on their own. The end result of all of this, of course, was a much more complex cell, with specialized intracellular compartments devoted to different functions: what we now refer to as a eukaryote.

Complexity can arise within a cell, too, because our molecular machinery makes mistakes. On occasion, it duplicates sections of DNA, entire genes, and even whole chromosomes, and these small changes to our genetic material can have dramatic effects. We saw how mutations can lead to a wide variety of phenotypic traits when we looked at how artificial selection has shaped dogs. These molecular accidents can even lead to complete innovation, like the various adaptations of flowering plants that I talked about in my last Evolution post. And as these innovations accumulate, species diverge, losing the ability to reproduce with each other and filling new roles in the ecosystem. While the creatures we know now might seem unfathomably intricate, they are the product of billions of years of slight variations accumulating.

Of course, while I focused this post on how complexity arose, it’s important to note that more complex doesn’t necessarily mean better. While we might notice the eye and marvel at its detail, success, from the viewpoint of an evolutionary lineage, isn’t about being the most elaborate. Evolution only leads to increases in complexity when complexity is beneficial to survival and reproduction. Indeed, simplicity has its perks: the more simple you are, the faster you can reproduce, and thus the more offspring you can have. Many bacteria live happy simple lives, produce billions of offspring, and continue to thrive, representatives of lineages that have survived billions of years. Even complex organisms may favor less complexity – parasites, for example, are known for their loss of unnecessary traits and even whole organ systems, keeping only what they need to get inside and survive in their host. Darwin referred to them as regressive for seemingly violating the unspoken rule that more complex arises from less complex, not the other way around. But by not making body parts they don’t need, parasites conserve energy, which they can invest in other efforts like reproduction.

When we look back in an attempt to grasp evolution, it may instead be the lack of complexity, not the rise of it, that is most intriguing.

Other Posts in the Evolution Series:

References

Ratcliff, W. C., Denison, R. F., Borello, M., & Travisano, M. (2012). Experimental evolution of multicellularity. PNAS Early Edition, 1–6. doi:10.1073/pnas.1115323109
Schwab, I. R. (2012). Evolution’s Witness: How Eyes Evolved. Oxford University Press, 297 pp.
Parker, A. (2003). In the blink of an eye. Basic Books, 352 pp.
Nilsson, D.-E. & Pelger, S. (1994). A Pessimistic Estimate of the Time Required for an Eye to Evolve. Proceedings: Biological Sciences Vol. 256, No. 1345, pp. 53-58
Reijnders, L. (1975). The origin of mitochondria. Journal of Molecular Evolution Vol. 5, No. 3, pp. 167-176. DOI: 10.1007/BF01741239

Evolution: Watching Speciation Occur | Observations

This is a repost from April 24^th, 2010. Watching Speciation Occur is the second in my Evolution series which started with The Curious Case of Dogs

We saw that the littlest differences can lead to dramatic variations when we looked at the wide variety in dogs. But despite their differences, all breeds of dogs are still the same species as each other and their ancestor. How do species split? What causes speciation? And what evidence do we have that speciation has ever occurred?

Critics of evolution often fall back on the maxim that no one has ever seen one species split into two. While that’s clearly a straw man, because most speciation takes far longer than our lifespan to occur, it’s also not true. We have seen species split, and we continue to see species diverging every day.

For example, there were the two new species of American goatsbeards (or salsifies, genus Tragopogon) that sprung into existence in the past century. In the early 1900s, three species of these wildflowers – the western salsify (T. dubius), the meadow salsify (T. pratensis), and the oyster plant (T. porrifolius) – were introduced to the United States from Europe. As their populations expanded, the species interacted, often producing sterile hybrids. But by the 1950s, scientists realized that there were two new variations of goatsbeard growing. While they looked like hybrids, they weren’t sterile. They were perfectly capable of reproducing with their own kind but not with any of the original three species – the classic definition of a new species.

How did this happen? It turns out that the parental plants made mistakes when they created their gametes (analogous to our sperm and eggs). Instead of making gametes with only one copy of each chromosome, they created ones with two or more, a state called polyploidy. Two polyploid gametes from different species, each with double the genetic information they were supposed to have, fused, and created a tetraploid: an creature with 4 sets of chromosomes. Because of the difference in chromosome number, the tetrapoid couldn’t mate with either of its parent species, but it wasn’t prevented from reproducing with fellow accidents.

This process, known as Hybrid Speciation, has been documented a number of times in different plants. But plants aren’t the only ones speciating through hybridization: Heliconius butterflies, too, have split in a similar way.

It doesn’t take a mass of mutations accumulating over generations to create a different species – all it takes is some event that reproductively isolates one group of individuals from another. This can happen very rapidly, in cases like these of polyploidy. A single mutation can be enough. Or it can happen at a much, much slower pace. This is the speciation that evolution is known for – the gradual changes over time that separate species.

But just because we can’t see all speciation events from start to finish doesn’t mean we can’t see species splitting. If the theory of evolution is true, we would expect to find species in various stages of separation all over the globe. There would be ones that have just begun to split, showing reproductive isolation, and those that might still look like one species but haven’t interbred for thousands of years. Indeed, that is exactly what we find.

The apple maggot fly, Rhagoletis pomonella is a prime example of a species just beginning to diverge. These flies are native to the United States, and up until the discovery of the Americas by Europeans, fed solely on hawthorns. But with the arrival of new people came a new potential food source to its habitat: apples. At first, the flies ignored the tasty treats. But over time, some flies realized they could eat the apples, too, and began switching trees. While alone this doesn’t explain why the flies would speciate, a curious quirk of their biology does: apple maggot flies mate on the tree they’re born on. As a few flies jumped trees, they cut themselves off from the rest of their species, even though they were but a few feet away. When geneticists took a closer look in the late 20th century, they found that the two types – those that feed on apples and those that feed on hawthorns – have different allele frequencies. Indeed, right under our noses, Rhagoletis pomonella began the long journey of speciation.

As we would expect, other animals are much further along in the process – although we don’t always realize it until we look at their genes.

Orcas (Orcinus orca), better known as killer whales, all look fairly similar. They’re big dolphins with black and white patches that hunt in packs and perform neat tricks at Sea World. But for several decades now, marine mammalogists have thought that there was more to the story. Behavioral studies have revealed that different groups of orcas have different behavioral traits. They feed on different animals, act differently, and even talk differently. But without a way to follow the whales underwater to see who they mate with, the scientists couldn’t be sure if the different whale cultures were simply quirks passed on from generation to generation or a hint at much more.

Now, geneticists have done what the behavioral researchers could not. They looked at how the whales breed. When they looked at the entire mitochondrial genome from 139 different whales throughout the globe, they found dramatic differences. These data suggested there are indeed at least three different species of killer whale. Phylogenetic analysis indicated that the different species of orca have been separated for 150,000 to 700,000 years.

Why did the orcas split? The truth is, we don’t know. Perhaps it was a side effect of modifications for hunting different prey sources, or perhaps there was some kind of physical barrier between populations that has since disappeared. All we know is that while we were busy painting cave walls, something caused groups of orcas to split, creating multiple species.

There are many different reasons why species diverge. The easiest, and most obvious, is some kind of physical barrier – a phenomenon called Allopatric Speciation. If you look at fish species in the Gulf of Mexico and off the coast of California, you’ll find there are a lot of similarities between them. Indeed, some of the species look almost identical. Scientists have looked at their genes, and species on either side of that thin land bridge are more closely related to each other than they are to other species, even ones in their area. What happened is that a long time ago, the continents of North and South America were separated, and the oceans were connected. When the two land masses merged, populations of species were isolated on either side. Over time, these fish have diverged enough to be separate species.

Species can split without such clear boundaries, too. When species diverge like the apple maggot flies – without a complete, physical barrier – it’s called Sympatric Speciation. Sympatric speciation can occur for all kinds of reasons. All it takes is something that makes one group have less sex with another.

For one species of Monarch flycatchers (Monarcha castaneiventris), it was all about looks. These little insectivores live on Solomon Islands, east of Papua New Guinea. At some point, a small group of them developed a single amino acid mutation in the gene for a protein called melanin, which dictates the bird’s color pattern. Some flycatchers are all black, while others have chestnut colored bellies. Even though the two groups are perfectly capable of producing viable offspring, they don’t mix in the wild. Researchers found that the birds already see the other group as a different species. The males, which are fiercely territorial, don’t react when a differently colored male enters their turf. Like the apple maggot flies, the flycatchers are no longer interbreeding, and have thus taken the first step towards becoming two different species.

These might seem like little changes, but remember, as we learned with dogs, little changes can add up. Because they’re not interbreeding, these different groups will accumulate even more differences over time. As they do, they will start to look less and less alike. The resultant animals will be like the species we clearly see today. Perhaps some will adapt to a lifestyle entirely different from their sister species – the orcas, for example, may diverge dramatically as small changes allow them to be better suited to their unique prey types. Others may stay fairly similar, even hard to tell apart, like various species of squirrels are today.

The point is that all kinds of creatures, from the smallest insects to the largest mammals, are undergoing speciation right now. We have watched species split, and we continue to see them diverge. Speciation is occurring all around us. Evolution didn’t just happen in the past; it’s happening right now, and will continue on long after we stop looking for it.

Soltis, D., & Soltis, P. (1989). Allopolyploid Speciation in Tragopogon: Insights from Chloroplast DNA American Journal of Botany, 76 (8) DOI: 10.2307/2444824
McPheron, B., Smith, D., & Berlocher, S. (1988). Genetic differences between host races of Rhagoletis pomonella Nature, 336 (6194), 64-66 DOI: 10.1038/336064a0
Uy, J., Moyle, R., Filardi, C., & Cheviron, Z. (2009). Difference in Plumage Color Used in Species Recognition between Incipient Species Is Linked to a Single Amino Acid Substitution in the Melanocortin?1 Receptor The American Naturalist, 174 (2), 244-254 DOI: 10.1086/600084
Phillip A Morin1, Frederick I Archer, Andrew D Foote, Julie Vilstrup, Eric E Allen, Paul Wade, John Durban, Kim Parsons, Robert Pitman, Lewyn Li, Pascal Bouffard, Sandra C Abel Nielsen, Morten Rasmussen, Eske Willerslev, M. Thomas P Gilbert, & Timothy Harkins (2010). Complete mitochondrial genome phylogeographic analysis of killer whales (Orcinus orca) indicates multiple species Genome Research

Image Credits:

Salsify plate showing two new species from the New Zealand Plant Radiation Network (taken from Ownbey, 1950 in which the species were described)

Flycatchers image by Robert Boyle, as featured on Science Now

Evolution: The Curious Case of Dogs | Observations

This is the first in a series of post of mine about Evolution that I started posting in January of 2010. I’ll be reposting the series over the next two months, culminating in a brand new post for the set in Jan 2012! I’m excited. You know you’re excited. Enjoy!

Man’s best friend is much more than a household companion – for centuries, artificial selection in dogs has made them prime examples of the possibilities of evolution. A century and a half ago, Charles Darwin recognized how the incredibly diverse dogs supported his revolutionary theory in his famous book On The Origin Of Species. At the time, he believed that dogs varied so much that they must have been domesticated from multiple canine species. Even still, he speculated that:

if… it could be shown that the greyhound, bloodhound, terrier, spaniel and bull-dog, which we all know propagate their kind truly, were the offspring of any single species, then such facts would have great weight in making us doubt about the immutability of the many closely allied natural species

If only Darwin knew what we know now, that indeed, all dogs did descend from one species!

While humans have been breeding dogs for over ten thousand years, it was until recently that strict standards and the emphasis on “purebreds” has led to over 400 different breeds that are some of the best examples of the power of selection. Those that doubt whether small variations in traits can lead to large levels of diversity clearly haven’t compared a Pug to a Great Dane – I mean, just look at them compared to their ancestor:

We’ve turned a fine-tuned hunting animal, the wolf, into a wide variety of creatures, from the wolf-looking shepherds to the bizarre toy breeds. Before domestication, dog’s life was tough. But when people pulled specific wolves out of their packs and began breeding them, we changed everything. There were some traits that made this easy – the social structure of wolves, for example, made them predisposed to belonging to a community. Still, we opened up a number of genetic traits and allowed them to express variety that would have been fatal in the wild. We not only allowed these traits to persist, we encouraged them. We picked dogs that were less aggressive or looked unique. And in doing so, we spurred on rapid diversification and evolution in an unbelievable way.

Take their skulls, for example. Like other members of the order Carnivora, dog’s skulls have a few distinctive characteristics: relatively large brains and a larger-than-normal structure called a zygomatic arch which allows for bite power and chewing. But years of hand-picked puppies has led to an amazing amount of skull diversity in dogs. A study recently compared the positions of 50 recognizable points on the skulls of dogs and compared them to each other and other members of the order Carnivora. They found that there was as much variety in the shape of the skulls of dogs as in the entire rest of the order, and the extremes were further apart. What does that mean, exactly? It means that the differences between the skulls of that Pug and Great Dane I mentioned before (on R) are greater than the differences between the skulls of a weasel and a walrus. Much of this variation is outside the range of the rest of the order, meaning dogs’ skull shapes are entirely unique. In just a few centuries, our choices have created unbelievable variety in the heads of dogs – more than 60 million years has created in the rest of the carnivores.

The amazing diversity of dogs is a testimonial to the possibilities of selection. And it’s not just their skulls that vary. A joint venture between the University of Washington and the Veterinary School at UC Davis mapped the variation in the genomes of a mere 10 different breeds of dogs. They found that at least 155 different regions of the dog’s genome show evidence of strong artificial selection. Each region contained, on average, 11 genes, so it’s harder to identify exactly what about each area was under the most selection, though there were clues. About 2/3 of these areas contain genes that were uniquely modified in only one or two breeds, suggesting they contain genes that are highly breed-restricted like the skin wrinkling in the Shar-Pei. Another 16 had variations in 5 or more breeds, suggesting they encode for traits that are altered in every breed, like coat and size.

While we usually think of evolution as a slow and gradual process, dogs reveal that incredible amounts of diversity can arise very quickly, especially when selective pressures are very, very strong. It’s not hard to see how selection could lead to the differentiation of species – just look at the breeds of dogs that exist today. There’s a reason that you don’t see many Chihuahua/Saint Bernard mixes: while it’s entirely possible for their genetics to mix, it’s just physically difficult for these two breeds to actually do it. Just imagine what a poor Chihuahua female would have to endure to give birth to such a mix, or how hard it would be for male Chihuahua to mount a female Saint Bernard. Indeed, dogs are well on their way to speciation.

Of course, it’s at this point that I have to mention that while I have talked about “dogs” this entire time, they’re not actually a different species. Wolves are Canis lupus, while dogs are merely a subspecies of wolves, Canis lupus familiaris. Despite centuries of selective breeding and the vast array of physical differences, dogs are still able to breed with their ancestors.

When you take away the selective breeding done by humans, a number of these unique traits disappear. But feral dogs don’t just become wolves again – their behaviors and even looks depend greatly on the ecological pressures that surround them. Our centuries of selective breeding have opened a wide variety of traits, both physical and behavioral, that may help a stray dog survive and breed.

A good example of what happens to dogs when people are taken out of the picture can be found in Russia’s capital city. Feral dogs have been running around Moscow for at least 150 years. These aren’t just lost pets that band together – these dogs been on their own for awhile, and indeed, any poor, abandoned domesticated canine will meet an unfortunate fate at the hands of these territorial streetwalkers. Moscow’s dogs have lost traits like spotted coloration, wagging tails and friendliness that distinguish domesticated dogs from wolves – but they haven’t become them. The struggle to survive is tough for a stray, and only an estimated 3% ever breed. This strong selective pressure has led them to evolve into four distinct behavioral types, according to biologist Andrei Poyarkov who has studied the dogs for the past 30 years. There are guard dogs, who follow around security personnel, treating them as the alpha leaders of their packs. Others, called scavengers, have evolved completely different behaviors, preferring to roam the city for garbage instead of interacting with people. The most wolf-like dogs are referred to as wild dogs, and they hunt whatever they can find including cats and mice.

But the last group of Moscow’s dogs is by far the most amazing. They are the beggars, for obvious reasons. In these packs, the alpha isn’t the best hunter or strongest, it’s the smartest. The most impressive beggars, however, get their own title: ‘metro dogs’. They rely on scraps of food from the daily commuters who travel the public transportation system. To do so, the dogs have learned to navigate the subway. They know stops by name, and integrate a number of specific stations into their territories.

This dramatic shift from the survival of the fittest to the survival of the smartest has changed how Moscow’s dogs interact with humans and with each other. Beggars are rarely hit by cars, as they have learned to cross the streets when people do. They’ve even been seen waiting for a green light when no pedestrians are crossing, suggesting that they have actually learned to recognize the green walking man image of the crosswalk signal. Also, there are fewer “pack wars” that once were commonplace between Moscow’s stray canines, some of which used to last for months. However, they remain vigilant against the wild dogs and wolves that live on the outskirts of the city – rarely, if ever, are they permitted into Moscow. When politicians thought to remove the dogs, their use as a buffer against these animals was cited as a strong reason not to disturb them.

Moscow’s exemplary dogs show how different traits help dogs adapt to different ecological niches – whether it be brute strength for hunting in the truly feral wild dogs or intelligence in the almost-domesticated beggars. Some wonder if the strong selection for intellect will make Moscow’s metro dogs into another species all together, if left to their own devices.

Dogs make it easy to understand and demonstrate the core principles of evolution – variation and selection – and how they can make such a dramatic impact on an animal. It’s no wonder that Darwin took cues from domesticated animals when formulating his theory of evolution. However, there’s still a lot to learn about the processes that have shaped our best friends, and what future lies for them. How much time will it take to completely separate dogs from wolves, into their own species? What areas of the genome are key to doing so? In studying dogs and wolves, we may gain insight into how speciation occurs and when a threshold of change is met for it to do so. Seeing how much change has occurred already makes you wonder what surprises our canine companions still have in store for us as they, and we, continue to evolve together over the next ten thousand years.

Citations:

Drake, A., & Klingenberg, C. (2010). Large Scale Diversification of Skull Shape in Domestic Dogs: Disparity and Modularity The American Naturalist DOI: 10.1086/650372

Akey, J., Ruhe, A., Akey, D., Wong, A., Connelly, C., Madeoy, J., Nicholas, T., & Neff, M. (2010). Tracking footprints of artificial selection in the dog genome Proceedings of the National Academy of Sciences, 107 (3), 1160-1165 DOI: 10.1073/pnas.0909918107

Poyarkov, A.D., Vereshchagin, A.O., Goryachev, G.S., et al., Census and Population Parameters of Stray Dogs in Moscow, Zhivotnye v gorode: Mat-ly nauchno-prakt. konf. (Proc. Scientific and Practical Conf. Animals in the City ), Moscow, 2000, pp. 84 87.

Vereshchagin, A.O., Poyarkov, A.D., Rusov, P.V., et al., Census of Free-Ranging and Stray Animals (Dogs) in the Coty of Moscow in 2006, Problemy issledovanii domashnei sobaki: Mat-ly soveshch (Proc. Conf. on Problems in Studies on the Domestic Dog), Moscow, 2006, pp. 95 114.