Decoding Our Family

This year has been a significant one in the world of primatology.  Field and lab studies have revealed insight into the origins of bipedalism, cultural complexity, tool construction and shelter construction.  However, the biggest news has come from genetics: the last two great ape genomes (gorilla and bonobo) were sequenced in their entirety (the first human genome was sequenced in 2000, the first chimp genome was sequenced in 2005 and the first orangutan genome was sequenced in 2011).  So now that the human genome and all of the great apes genomes have been sequenced, what have we learned?  Did genome sequencing reveal any surprises about our evolutionary history with our closest relatives?  Well, I’m going to try and break down some of the deepest evolutionary insights gained from decoding our family.

Evolutionary history

Decoding the human and great ape genomes has finally given us definitive answers regarding great ape relatedness and critical past speciation events.  During the 19th and early 20th century many evolutionary theorists could tell that great apes were our closest relatives but there was still debate regarding who we were most closely related to and what continent our species evolved on.  Although Charles Darwin believed our closest relative was the chimpanzee and our home continent was Africa, others thought our closest relative was the orangutan and our home continent was Asia, and embarrassingly, some argued that our home continent was Europe based on the fraudulent Piltdown Man skull.

Throughout the 20th century, phenotypic and geographical evidence from known fossil humans indicated that our closest common ancestor was with chimpanzees and bonobos and our home continent was Africa, however, since sequencing all great ape genomes, we now have the undeniable proof.  For example, the genome sequencing attempts has revealed that we differ from chimpanzees and bonobos equally by 1.3%, while we differ from the Asian orangutans by 3%.  Interestingly, we also gained insight into relationships between the great apes themselves, for example we now know that chimpanzees and bonobos only differ by 0.4% of their genomes.

Now I must take a second to note that simply knowing the percentage two organisms differ isn’t all that is important about the genome; it is also important to know:

  • What genes are being activated at what time during development
  • Percentage of genetic difference or similarity that is from ‘junk DNA’ (DNA that does not code for anything)
  • Specific information on what is different about the genes that are not shared and when they were selected for

There are several great examples of why it is important to know this information, instead of simply relying on the overall percentage of genetic similarity:

  • All breeds of dog differ very little (<0.2%) in overall genetic sequence variation yet show considerable phenotypic variation
  • Chimpanzees and humans have the same amount of overall genetic sequence variation as the two mouse species, Mus musculus and Mus spretus, yet those two mouse species look identical, whereas chimpanzees and humans differ substantially in phenotypic variation
  • And my all-time favourite – humans are about 50-60% genetically similar to a banana

However, knowing the difference our genomes vary is still an important piece of knowledge, because it does show us the overall pattern of relatedness and allows us to estimate timing of speciation events.  Before all the great apes had their genomes sequenced best estimates on speciation dates were drawn from fossil evidence (which are almost non-existent for our closest relatives).  From this evidence general consensus was that our common ancestor with chimpanzees and bonobos split 4 million years ago (mya), our common ancestor with gorillas split 8 mya and our common ancestor with orangutans 12 mya.  Now that we can compare genomes, these dates have all been adjusted and pushed back.  The genetic evidence indicates that we share a common ancestor with chimpanzees 6 mya, gorillas 10 mya, and orangutans 15mya.

So the picture of our evolutionary past has become a lot clearer because of the genetic evidence.  This has implications for palaeoanthropology because it means that we now have a strict window for investigating candidate common ancestor species with our closest living relatives.  It also means that species we considered candidates in the past (e.g., Lucy (Australopithecus afarensis)) have now been reintegrated into a new narrative of human evolution that extends its roots back an extra 2 million years.

Here are a list of species we have found around the temporal range we would expect the speciation event to have occurred:

Sahelanthropus tchadensis (7mya) (Central Africa)
Orrorin tugenensis (6mya) (Eastern Africa)
Ardipithecus kadabba (5.8-5.2mya) (Eastern Africa)
Ardipithecus ramidus (4.5-4.3mya) (Eastern Africa)

Orrorin is looking pretty good at the moment.

Pace and quirks from the past

But the genome sequencing taught us more than just relatedness and speciation events.  The evidence can also give us insight into the pace of evolution and some interesting evolutionary quirks hidden in our genes.

For example, the orangutan genome has shown us that the pace of evolution for them has been glacial, whereas the pace of evolution for chimpanzees, bonobos and humans has been comparatively fast.  There are several hypotheses that have been suggested to explain these findings.  It could be that orangutan evolution has been slow because both species of orangutan have been isolated on islands throughout their history (Sumatra and Borneo) and consequently, neither species has needed to adapt to a significantly different environment.

Analysis of the genomes has also shown us that some speciation events have been messier than others.  For example the bonobo-chimp split seems to have been very sudden, abrupt and clean.  This means that when the common ancestor of the chimpanzee and bonobo split there was no further interbreeding.  This lends support the hypothesis that Congo River acted as a natural barrier to migration for both chimpanzees and bonobos.  However, we do know that not all speciation events were so clean.  In fact, the human-chimp-bonobo split appears to have been far less abrupt and may have been a slow speciation that spanned a million years or more.  This means that a permanent ecological barrier was likely not responsible for the speciation event.

Some odd quirks of the past have also been revealed in the early years of great ape genome analysis.  Perhaps one of the more interesting finds is that gorillas and humans share a considerable number of functional genes that chimpanzees do not have.  One of these genes is LOXHD1  which is responsible for human hearing.  Researchers in the past hypothesized that this gene must have been selected for during the development of complex language.  However, if gorillas also possess this gene and it is expressed at similar frequencies, this cannot be the case, unless gorillas are keeping their ability to use complex language a secret.

Family decoded

Although our family has now been decoded there is still much more research to be completed and much more to know about our evolutionary history and our shared ancestry with the great apes.  Genomes are very large, and it is not clear what the function of all expressed genes is.  Furthermore, much of the questions that were answered by sequencing the great ape genomes have raised more complex questions that require more data and more hypothesis testing to resolve.  But one thing is clear, by decoding our family we have gained a better sense of who we are and where we came from.

 

A Conservation Story Gone Bad

Criticizing the way science is communicated to the public by various media platforms is not a new theme in The Ratchet (see: here and here).  Whenever I see something in the media I feel has been mischaracterized or would be misleading to people without background training in that discipline I tend to get upset and want to vent.

Unfortunately this happened again recently while I was watching a BBC documentary.  Now, I know what your thinking.  The BBC provides amazing science and nature programming.  How could I pick on the BBC?  Well, I didn’t necessarily want to pick on them, because they do usually provide amazing science and nature programming and I rarely find any fault in the way they communicate scientific information to the public.  However, I believe they recently released a dangerously simplistic Living with Baboons special.  This documentary is dangerously simplistic, not because of the primatological content communicated, but because of the portrayal of indigenous groups who must share land and resources with the baboons.

In the documentary you are introduced to biologist Mat Pines, the Hamadryas baboon population Pines has been following around for the past 5 years within Awash National Park, and the Afar tribe.

Pines seems to be a likeable and intelligent individual who has sacrificed a great deal personally and financially to live among baboons for five years.  He knows an incredible amount of detailed information about the population he studies — a type of knowledge that one could only acquire from living among the baboon group for years.  He seems to be passionate about all aspects of baboon life, and genuinely loves their individual personalities and unique adaptations to a savannah-highland lifestyle.

The Hamadryas baboons are shown in the documentary to be an exceptionally adaptable species that range for many kilometres throughout the day in groups of over 100 individuals.  The social complexity of their individual relationships is overwhelming but the documentary does give insight into their basic structure.  They were able to capture quite a diverse range of different situations and circumstances that show the complexity and range of baboon behaviour.

So far so good right?  Well, kind of.  Pines and his work to save the baboons form the basic skeleton of the narrative.  Pines is the loveable, selfless western protagonist.  And as the narrative develops it becomes clear who the antagonists in this narrative are: the Afar tribe.  Meet the gun-wielding, monkey-killing, barbaric Afar:

The BBC portrays these people to be irrational and combative actors in this conservation drama.  While Pines is the knowledgeable academic, fighting for ecological justice; the Afar are the savages, violently opposed to preserving our primate cousins for future generations of ecological stability and increased biodiversity.

But this constructed narrative is not the full story, and I believe the BBC did a poor job of communicating the complexities of the social dynamics in Awash National Park.  The Afar tribe, like almost all other human communities, are not illogical and irrational.  They constantly live on the verge of famine and death.  There are long periods during their year when resources they need to survive are simply unavailable.  As a consequence tensions run high between the Afar and any other group that competes and/or threatens to make their existence even harsher.  For this reason, baboons are seen as pests, not our cousins.  Baboons travel their land, raiding crops, consuming resources the Afar need.

So when Pines goes to village meetings with the Afar to attempt to tell them why baboons need to be saved, the Afar are obviously confused and disagree.  They find it weird that Pines lives with the baboons.  Why is he doing this?  What purpose does it serve?  These are logical and rational questions when understood from the perspective of the Afar.  How could they possibly understand that a man could follow around baboons for a living?  Almost everyone in their tribe must do something related to food production.  They do not have the global economy and infrastructure at their finger tips like many people in the west do.  In western society we can go to university, study an obscure subject unrelated to food production, and dedicate our lives to saving baboons, or studying the swarming behaviour of locusts, or the night ranging patterns of lemurs.  For the Afar, surviving long enough to see the next day is all they can do.  So when they see a man who is following around the baboons… they not only think the behaviour is crazy, but they think that he too is crazy.  And when they see a baboon stealing crops, they want to shoot it.  As I said, baboons are not precious pieces of Earth’s biodiversity to them; they are pests increasing their tribes chances of famine.

The BBC did not tell this story.  This was not in the narrative.  Was Pines to be blamed?  No.  Pines was doing his job and he should be commended for his dedication to conservation.  But in no way were the Afar portrayed fairly.  They were portrayed as savages who didn’t understand how we should exist with nature.  Conservation is important and it is important to communicate stories from the front lines of conservation work currently being done, but we should not demonize the poorest people on the planet while we do so.

The Evolution of Primate Sleep

St. Catherines Island studying ring-tailed lemur (Lemur catta) sleeping patterns I’ve learned a lot about the ecological determinants of lemur sleep site choice and nocturnal activity pattern.  While it was not planned, this is quite similar to what I studied as an undergraduate researching the environmental determinants of chimpanzee nesting in Cameroon.  As a consequence, I have become an unintended expert on primate sleeping patterns.  Also, because the two species I have studied are so distantly related phylogenetically within the primate order, it has made me aware of some interesting trends in the evolution of primate sleep.

First off let’s start with the basics.  Ring-tailed lemurs are prosimian primates that are part of a lemur clade of over 100 species.  All known extinct and extant members of the clade live(d) in Madagascar and have been evolving in isolation from all other primate species for almost 65 million years.  They are also one of the most primitive of all primate clades and closely resemble the stem primates, Plesiadapis.  In contrast, chimpanzees are part of the ape clade, which is composed of far fewer species than the lemur clade.  They live in populations that are distributed throughout most of sub-Saharan Africa and are thought to have evolved sometime within the past 6-8 million years (few known fossilized remains prevent a deeper understanding of this evolution).  Chimpanzees are one of the least primitive of all primates, and share only primate universal features with the stem primates, Plesiadapis (e.g., binocular vision, nails, opposable thumbs).

Quick side note: the word ‘primitive’ in primatology does not mean ‘less evolved’ or ‘less complex’ and is not seen as a derogatory term.  Primitive simply means resembling the ancestor.  So in this case lemurs are more primitive than chimpanzees because lemurs share more in common with the common ancestor of all primates than chimpanzees do:

However, primitive is a relative term.  Chimpanzees are more primitive than humans because chimpanzees more closely resemble the chimpanzee-human common ancestor than humans do.

This all has relevance to the evolution of sleep patterns because anatomical similarity can help us piece together the evolution of certain behaviours, including sleeping behaviours.  Throughout my research I have observed sleeping patterns that can tell us a lot about the general sleeping pattern that has developed throughout the 65 million years or so of primate evolution.  I believe some of these observations confirm what previous primatological work has discovered, and some observations may add a novel interpretation to the evolution of these sleeping patterns.

Quick note: Remember, these are patterns, and there are exceptions to these patterns.  I will try and acknowledge some of these exceptions to the general pattern, and try and hypothesize as to why certain behaviour patterns would have re-emerged.

Pattern #1

Throughout primate evolution most primates have been arboreal sleepers.  As humans are one of the most terrestrial primates, we can sometimes forget that most of our order consists of animals highly specialized for arboreal life.  And when it comes to sleep, primates will almost without exception opt to spend their sleeping hours in a tree, but not just any tree.  During my current field research it became obvious that the ring-tailed lemurs would only sleep in very specific trees:

They were always trees that were not only very high off of the ground, but also provided them with an added safety from terrestrial predators: no lower branches.  In my opinion, this is a biologically ingrained behaviour for ring-tailed lemurs (and most other lemurs).  In Madagascar most populations of lemurs are in constant danger from the cathemeral fossa.  Fossa’s are lemur hunting specialists that can climb trees and prey on lemurs in both the day and night.  On St. Catherines Island there are no fossas (or any terrestrial predators to take the fossas place) yet they will still not settle for sleeping trees with lower branches.  As I mentioned, most other primates (including monkeys and apes) behave the same way and much prefer to nest arboreally. For each primate there may be more complex and specific requirements for a sleeping site, but most primatologists agree that arboreal sleep has a specific anti-predator function.

However, for chimpanzees, although arboreal sleeping is certainly the norm in most groups, some individuals and some groups do relax their sleeping site requirements and sleep terrestrially.  This interesting break from the general primate pattern has implications for the development of human sleeping patterns because sometime in our evolutionary past we gradually came down from our arboreal niche and began attempting to live completely terrestrially.

During my time in Cameroon I observed that some chimpanzees were nesting terrestrially at night.  These happened to be chimpanzees who were also in an area with no human predation pressure (chimpanzees in areas with high levels of human predation pressure always nested arboreally).  This research made me realize that arboreal sleeping throughout primate history may have been primarily driven by predation pressure.  This could mean that our human ancestors began coming down from the trees due to living in an environment with relaxed predation pressure or they became better able at avoiding and preventing predation events (e.g., larger groups, control of fire, better weapons).

Although arboreal sleeping does offer many advantages, terrestrial sleeping allows for greater environmental flexibility and as a consequence enabled our ancestors to move from rainforests and wooded savannahs into different environments because we were no longer dependent on trees for safety.

Pattern #2

A second obvious pattern has to do with the evolution of nest-building or sleeping platform building.  It was no surprise while I was in the field on St. Catherines Island that I did not see any ring-tailed lemur build a nest to sleep in.  Almost no primates build nests to sleep in.  In fact, the only primates that build nests are the great apes.  Nest building is almost certainly a sign of advanced intellect in primates due to the highly social nature of the acquisition of nest building skills (unlike nest building in other species, or damn construction in beavers, which functions more as an extended phenotype).  Primate nests are highly complex structures that require a considerable amount of individual skill and social learning.

Nests also offer the great apes a few very important advantages.  They have been shown to decrease risk of disease when nesting arboreally and terrestrially, aid in thermoregulation in both extreme cold and heat and improve overall sleep quality.  This proved to be a key development in the evolution of primate sleep and may have developed as far back as 20 million years ago.  It was certainly a pattern that characterized our ancestors, as large complex nest-like structures have been found at sites associated with the earliest modern human populations in Africa (all terrestrial of course!).

Pattern #3

A final pattern that I feel deserves mention in this post is the distribution of sleep over a 24 hour period.  Throughout the course of primate evolution more and more primates began adapting to a diurnal existence.  Although ring-tailed lemurs are certainly more primitive than chimpanzees, they seem to have adapted to a primarily diurnal existence as well.  Despite this, there is growing evidence that they also spend a considerable amount of time nocturnally active, which may re-classify them into the odd cathemeral category.  Most of the other 100 or so lemurs are either nocturnal or cathemeral, which reflect their primitive adaptations to the dark half of the L/D cycle.  During my observations the ring-tailed lemurs were certainly night active at times.  They ranged occasionally and there were periods during the night when the entire group would be awake and active within their sleeping tree.

This type of behaviour is not typical of most monkeys and apes (with the notable exception of the aptly titled owl monkey).  At some point in the evolution of primate sleep (probably with the emergence of the first monkeys 40-30 million years ago), primates began occupying diurnal niches with increased frequency.  In contemporary times most monkeys and apes are rarely, if ever, active at night.  While I was in Cameroon this was evident in the ecological patterns left behind by chimpanzee groups.  They had specific nesting patterns for day and night use.  Day nests were simple and mostly terrestrial (even in areas with high human predation pressure).  Day nests were also constructed around termite mounds and ant hills, and surrounded with ‘fishing rods’ and play tools.  In contrast, night nests were far more complex, offering a more stable structure, more padding for comfort and constructed almost exclusively in trees (with some exceptions as previously mentioned).

Final thoughts

It has been an interesting journey learning about the world of primate sleep, and a happy coincidence that my observations and data happen to be on two very different species of primate.  As a consequence I have had a chance to see first hand how primate sleep has developed in distantly diverged clades.  In lemurs sleep is arboreal, with no nest and could be distributed during substantial periods of both the day and night.  In chimpanzees sleep can be both arboreal and terrestrial, always with a nest, and is exclusively distributed during the night.  These experiences have helped me understand our closest relatives, but they have also helped me understand the evolution of our own behaviours.  Now it is time for bed.

 

Diurnality, Nocturnality, and Cathemerality

Diurnality, nocturnality and cathemerality are all concepts that define different observed activity patterns in the animal kingdom.  In the classroom these concepts were all very clear and made perfect sense to me.  If an animal was primarily active during daylight hours and its circadian rhythm was intimately tied to the light half of the L/D cycle, it was diurnal.  If an animal was primarily active during the night and its circadian rhythm was intimately tied to the dark half of the L/D cycle, it was nocturnal.  And if an animal was not wedded to being active during either the day or the night, it was cathemeral.

However, the field is not the classroom and these concepts all become quite a lot more confusing when your observing and recording the activity patterns of a different species (in this case, ring-tailed lemurs (Lemur catta)).  But first, a little history.

Understanding activity patterns

For several decades early primatologists (and other animal behavioural specialists) assumed that all animals were either diurnal or nocturnal.  Furthermore, they believed that these two activity patterns were uniquely distinctive characteristics of the two primate suborders: strepsirrhini (lorises, galagos and lemurs) were nocturnal and haplorhini (tarsiers, monkeys, apes and humans) were diurnal.  However, this was largely a product of researcher bias and the way primatologists divided up their field seasons.  Typically, it was convention for a primatologist to study an animal either in the night or the day.  Rarely, would researchers decide to track and follow a primate throughout a 24-h period or design a more erratic observational time schedule that was dispersed both during the day and the night.

Nor was this seen as necessary.

Primatologists who studied bonobos or baboons (for example) assumed that their animals were active only in the day and that they only slept at night.  Likewise, researchers who studied mouse lemurs or pottos (for example) knew that their study subjects were active during the night and were sleeping during the day.  The need for the concept of cathemerality was not thought to be necessary until it was discovered that members of the genus Eulemur did not fit into either category.

This proved to be an evolutionary riddle for biologists and anthropologists as well.  Why would an animal become adapted to both the day and the night?  These are vastly different temporal niches that require exceptionally specialized sensory structures (primarily optical).  Being active during both the night and day would require adapting partially to both time periods at the expense of becoming biologically specialized in one.  How could such a generalist compete with diurnal and nocturnal specialists?  In some ways these questions have not been answered and are still being debated by contemporary researchers.

Cathemerality was also problematic because it destroyed the simplistic notion that all of the most primitive primates were nocturnal and that divergent evolution had provided our order with a very linear progression of ‘higher’ primates that had become steadily more diurnal.

Either way, over the past few decades all animal behavioural researchers have had to accept that the world of animal activity patterns is not black and white and different evolutionary pressures can force any animal into either temporal niche, with cathemeral behaviour possibly being a transition stage into complete diurnality or complete nocturnality.

So why so confused?

The reason this makes studying activity patterns confusing is because of the inherent limitations and subjectivity of concepts and definitions.  Without releasing exact data, I can say that I have definitely observed periods when the lemurs have been awake at night.  They will do anything from lifting their head and surveying the area around them to social grooming to play to switching sleeping trees to a nearby tree.  So there is a range of activity, and there may even by a pattern to this activity.  Is that cathemerality?  Am I right to conclude that thus far I don’t believe I’ve witnessed it?

Unfortunately, it may depend on the definition of the concept of cathemerality.  Some researchers will say that in order for an animal to be classified as cathemeral, their activity needs to be distributed ‘fairly evenly’ throughout the 24-h period, whereas others will say cathemerality is an activity pattern comprised of ‘distinct periods’ of nocturnal and diurnal behaviour.  Of course, these definitions are likely used by different researchers in order to gain a more favourable research conclusion or to make publication easier.  If in order to classify as cathemeral activity the animal must distribute activity ‘fairly evenly’ throughout the 24-h period, then I certainly have not witnessed that pattern.  However, have I witnessed ‘distinct periods’ of activity in both the diurnal and nocturnal temporal niches?  I think I could conclude ‘yes’ objectively.  But then I would become troubled because couldn’t most animals be considered cathemeral?  In my mind that interpretation sort of distorts the usefulness of the category.

But then again I have further questions about these categories while observing at night.  Is an animal cathemeral if they continue foraging and travelling past dusk but then go to sleep shortly after dusk and then sleep continuously until dawn?  Is an animal cathemeral if an animal is awake for parts of the night but their behaviour is radically different and substantially less active than during the day?  Is an animal cathemeral if they are only active at night during a few days or weeks out of a year?

This seems to bring me back to a problem that I’ve acknowledged before in The Ratchet about concepts and definitions.  Humans universally attempt to make our world discontinuous, when really it is continuous and cannot be categorized.  There is a range of activity patterns in the animal kingdom that cannot be nicely grouped into three categories: diurnal, nocturnal and cathemeral.  Even if, by current primatological standards, I would be able to claim in a research article that ring-tailed lemurs are cathemeral, with the current data I have it would be obvious that their activity budget would be drastically different than previous species who have been classified as cathemeral.  For me this is not only a problem in the field, but it raises questions about the way knowledge is produced and disseminated.  And I am still unsure about how I will solve this problem internally when I begin writing my thesis.