The evolution of complexity is an absolutely fascinating topic and there have been multiple,

significant and irreversible jumps in complexity that have happened throughout the history

of life, such as going from prokaryotes to eukaryotes, or unicellular organisms to multicellular

organisms.

These are known as major evolutionary transitions, and today, with the help of Professor Jacobus

Boomsma (or Koos) we are going to be talking about how one of the most recent evolutionary

transitions happened, how we went from solitary insects to cooperative superorganisms.

[INTRO by Caro Waro & Cristina de Manuel]

For those wondering, a superorganism is a colony of individuals with irreversibly differentiated

castes, and a prime example of that would be the honeybee hive.

Honeybee colonies actually have three differentiated castes:

the drones whose sole purpose is to mate with the queen, the queen, who will store the drone's

sperm for the rest of her life and use it to fertilise her eggs, and the workers, who

don't reproduce and whose sole duty is to maintain the nest and feed the queen and the

brood to ensure the colony is maintained.

Within a superorganism, there is a distinct and irreversible separation between reproductive

individuals and those who are sterile.

In essence, a superorganism actually lives and reproduces as if it were an entire organism

in itself.

Superorganisms are actually considered a form of obligate eusociality, and eusociality,

which means "true sociality" has actually evolved repeatedly within many animals, and

basically, some animals actually opt out of reproducing in lieu of helping another individual

reproduce in its place.

Eusocial animals share various key characteristics.

They have overlapping generations, in which the parents and the offspring coexist together,

which leads to cooperative breeding and reproductive altruism, which basically means that some

individuals do not reproduce in lieu of helping other individuals reproduce more.

The transition from facultative eusociality, in which some individuals can switch between

castes, for instance, sterile workers could turn into potential reproductive individuals,

into obligate eusociality, where such switching is not possible because you're committed to

life to the caste you belong to, has believed to have evolved four times: in the higher

termites, the vespine wasps, the corbiculate bees and the ants.

However, it has been a bit of a mystery why this evolution would take place in the first

place, and Professor Koos Boomsma, who is the Director for the Centre of Social Evolution

in the University of Copenhagen and recently was a visiting Newton Abraham's Professor

here at Oxford - is actually the father of the accepted theory of how a superorganism

could evolve in the first place.

Koos: "Well, the idea I've been developing over the last ten years is that what you need

for that is the most strict form of lifetime monogamy that you can imagine.

That is, a form of monogamy where you only will have one sexual partner in your life

and you will die with that partner"

The idea of lifetime monogamy is extremely important due to the key idea of relatedness.

Now, inclusive fitness and relatedness are very important concepts in this video.

I have actually made a video [4mins] and a blogpost before on these topics, so if you've

never heard of it, I would recommend watching it to get a better understanding.

But in short, individuals seeks to maximise inclusive fitness.

What that means is that an individual doesn't maximise its direct fitness which would imply

that it has as many offspring as possible, but rather that it maximises a combination

of having as many offspring as it can and also helping individuals that share the same

genes that they do.

So this means that an individual might be more likely to help a relative because they

will share genes together at a higher rate than the population average, and that rate

is what is known as relatedness.

Now, the higher the relatedness between two individuals, the higher the proportion of

genes they share as compared to the population average, and in the context of proto-colonies,

if relatedness is sufficiently high that an individual has the same relatedness to their

own offspring as they do to their siblings, the potential for caste evolution begins to

arise, as some individuals could opt out of reproducing in order to help a dominant reproductive

to produce more offspring.

Koos: "And that means that there is essentially no conflict between two parents if that happens.

And that also means that there will be 100% families that only produce full siblings,

and that makes your relatedness between those siblings and their future siblings so high,

maximally, invariably high, that it becomes indifferent in relatedness terms whether you

breed yourself or whether you actually help your mother producing more brothers and sisters"

Now, how lifetime monogamy is maintained in these proto-colonies can actually occur in

different ways.

For instance, in the Hymenopterans, which are the bees, the wasps and the ants, what

happens is the queen mates a single time with the drone.

After mating, the male generally dies, and the queen goes on to found a colony alone.

She will then store his sperm for the next 30 years (in some ant spp, honeybees last

around 5 years) from which she produces all of the eggs, from which the rest of the colony

will arise.

Koos: "Now the termites have done it in a slightly different way, there the father of

the family survives, they [mother and father termite] dig in together, so they have had

their dispersal flight and then they find each other, but rather than mating and the

male dying as happens in the ants, bees and wasps, here they basically form a tandem pair,

and they find a place to dig in together.

They will then make a royal cell and mate, and mate repeatedly over time, and that will

produce the offspring and the offspring will start doing the foraging and getting the food

to the colony, so the colony can grow, and some of these termites become enormous, just

like some ant colonies, but they are, interestingly, the pair will be together, throughout their

long lives"

Either way, lifetime monogamy is enforced such that the queen mates a single time in

her life and the workers never have the opportunity to mate.

The consequence is that the colony's relatedness is maximised, and as long as the relatedness

between offspring and siblings is maintained at a exact constant of 0.5 or above, evolution

will eventually select for worker sterility.

This selection will occur as soon as the fitness benefits of the colony outweigh the costs,

as long as relatedness remains at a invariable 0.5.

This period of time in evolutionary history is known as the monogamy window.

Now, in addition to worker sterility, lifetime monogamy also selects for extraordinarily

long lifespans.

You'll probably know that the queens of these reproductive castes often live for many decades

(ants, years in bees), but it does mean that when they do die, or if their sperm storage

runs out, the colony will die with it because there will be no one there to replenish the

workers.

Koos: "The whole colony will perish, because you need them both.

Just like in an ant queen, if she would run out of stored sperm, that's the end of it"

And unlike unfacultative eusocial animals there will be no individual that can take

on the reproductive role after one has died - such as the case of the naked mole rats.

Naked mole rats live in colonies, with one reproductive queen who produces the offspring,

one to three males they mate with and the workers, who are sterile and help maintain

the nest and forage for food.

However, the difference between naked mole rats and obligately eusocial animals is that

when the queen of the naked mole rat dies, the most dominant worker becomes the new reproductive.

Their castes are reversible.

Now I'm sure there'll be someone out there who will say, "By the way Inés, you are aware

that there are plenty of superorganisms out there that have a relatedness of way less

than 0.5 and that have no form of lifetime monogamy?" and indeed you'd be absolutely

right, there are plenty of examples: honeybees for instance, the queens actually

mate with anything between one and forty drones on the nuptial flight, and ants often have

what is known as polygynous queens, which means that multiple queens found the nest.

However, what I've been trying to explain in this video is that in order for major evolutionary

transitions to happen, where you end up with a superorganism, and irreversibly differentiated

castes, all you need is to have a period of time where you've gone through this period

of lifetime monogamy and that relatedness settling at around 0.5.

After that transition has happened, by nature, it is irreversible so it's normal for secondary

developments to happen.

And, to be honest, being able to mate with multiple individuals and have a higher genetic

diversity is a great way of being robust to disease and environmental fluctuations.

Koos: "Those colonies tend to be more robust against diseases, so they simply tackle challenges

from infections more efficiently than colonies that are full siblings, and again, you can

imagine, particularly in societies that become really big and long-lived that that is a significant

advantage"

On many levels, the evolution of superorganisms share many parallelisms with zygote development.

Koos: "You can compare say the cells in my body in some ways with worker ants serving

their colony, the only difference is that they're all fixed together in my body whereas

ant workers walk around doing their things.

But they're very similar in their loyalties and my skin cells, my brain cells, and my

stomach cells are all totally devoted to keeping me alive and as long as they possibly can

and that's exactly the same for ant workers, and when I thought about it, I realised that

in fact the origin of a body, let's say, my body, or a horse or an elephant, or little

mice, is very similar to a monogamous situation because single zygotes, it's a lifetime commitment

to an egg produced by my mother and a sperm produced by my father and when they came together

and fertilization took place, that was a lifetime commitment, that sperm could not have regretted

the commitment and rather have fertilised another egg, neither could that egg have thrown

out that particular sperm because it didn't particularly like it and would've liked to

have another one.

So that is why I think that evolution of multicellularity, things like animals, plants, some algae and

the higher fungi - we can explain these major transitions with very much the same simple

logic, strict lifetime commitment at the foundation"

I find it beautiful how the way superorganisms evolved in entirely analogous to all previous

major evolutionary transitions, and this is actually a collaboration with Stated Clearly

so I urge you to learn more about over here in Stated Clearly's impeccably animated video

on how the other major transitions of evolution happened.

I also really want to thank Professor Koos Boomsma who kindly agreed to be interviewed

for this video.

Now the actual interview lasted over an hour in length, we chatted about lots of things

about eusociality and the evolution of bees, and a month ago I asked people to send me

questions on twitter about the evolution of bees and eusociality, so I'll probably release

that part of the interview where he's answering susbcriber-submitted questions in that part

- but - as you may have twigged, this is one of my favourite areas in evolutionary biology

so if you have any questions on the topic feel free to ask them down below, I will definitely

answer and who knows, I might even make a follow-up to this video.

And as always, thank you so much for watching me and I'll see you in the next one, bye!

[Channel Art and Animation by Caro Waro and Cristina de Manuel]

[Music by Thastor and Cryosleepkitten] [Hosting, Scripting, Editing: Inés Dawson]

[Special thanks to Prof. Boomsma for being interviewed]

[Translated by {your name} into {language}]