- Hello.
I am Dr. Nelson Scottgale,
a member of the Darwin Festival Committee.
Welcome to the third day of the 42nd Annual
Darwin Festival at Salem State University.
I would like to now turn the microphone over
to Dr. Juditha Burchsted for her introduction.
Thank you very much.
- Good afternoon, and welcome to the Founders' Lecture
of the 42nd Annual Darwin Festival
at Salem State University.
Our founders' lecture honors
Philip DePalma and Virginia Keval,
two professors at Salem State,
who 41 years ago found a way
to bring the evolutionary foundation of modern biology
to their students in their human and social biology course.
The fact that the annual Darwin Festival not only continues
at Salem State, but serves as a model for a growing number
of commemorations throughout the world
is a testament to their farsightedness,
as well as their ability to inspire
their students and colleagues.
Sadly, Phil DePalma is no longer with us,
but we are very honored by the presence
and continued support of our emerita professor
Virginia Keval who organized the Darwin Festival
for 20 years and joins us in our webinar today.
Also joining us remotely is emerita professor
Susan Case, who spoke at the inaugural festival,
before joining the Biology Department,
and organized the Darwin Festival
after professor Keval's retirement.
Ginger and Sue,
your shared commitment to the Darwin Festival
inspires us all.
Thank you so much.
Today, I am very pleased to welcome
as our founders' lecture speaker, evolutionary biologist,
Maydianne Andrade.
Dr. Andrade is a Professor
in the Department of Biological Sciences
at the University of Toronto Scarborough,
and in the Graduate Department
of Ecology and Evolutionary Biology
at the University of Toronto.
She earned her PhD in neurobiology and behavior
from Cornell University investigating the evolution
of cannibalistic mating behavior
of black widow spiders,
research she continues in both lab and field work.
She has received numerous teaching and research awards
including a prestigious Canadian research chair
in integrative behavioral ecology.
Dr. Andrade was elected a Fellow
of the Animal Behavior Society,
and the American Academy of Arts and Sciences.
The Darwin Festival is very pleased to give a warm welcome
to Dr. Maydianne Andrade for our founder's lecture,
entitled Through a Web, Darkly:
Sex, Death, and Adaptation in Widow Spiders.
- Thank you so much for that kind introduction,
and for inviting me here today, it's an honor.
This really is one of the longest Darwin Festivals.
And as you'll see, Darwin inspired my entry into science,
and I wanna talk to you a little bit about
where that started and where I'm going.
So in one of the memes of 2020, how it started.
It started with a fascination as an undergraduate
with sexual cannibalism.
And at least initially it was in terms of cannibalism
in praying mantis, which you see here on the left,
and now on the right,
a video of mantis by Dr. William Brown and Phil Hastings
at SUNY Fredonia.
Now sexual cannibalism is fascinating.
It has fascinated scientists for quite a long time.
This quote being from 1886,
describing what happens after a male and female mantis
were left together in a lab.
"She had completely rid herself of her spouse
"by the morning after the time they were paired
"and nothing but his wings remained."
Now, why did this deliver entree to evolutionary biology?
Well it was puzzling, and it was puzzling not just because
males were regularly killed
by potential partners during mating,
but also because there's actually a ganglion,
a cluster of nerve cells in the male's thorax, upper body.
And when the female begins to eat the male,
typically from the head down,
that ganglion is removed,
and actually results in more vigorous copulatory behavior
than if it had been intact.
That is, people speculated,
that males were actually adapted for being killed.
That idea was one that had some legs
for a while in the popular literature,
but it wasn't until the 1980s
that Ruth Buskirk and her colleagues
asked whether mathematically,
whether in terms of our actual theoretical understanding
of evolutionary biology, something like this could evolve.
And they wrote a paper in the 80s,
called the Natural Selection of Sexual Cannibalism
that proposed and showed quantitative theoretical arguments
to support the idea that you could actually get
the evolution of males,
that not only just didn't manage to avoid being killed,
but actually had become adapted
to allowing females to kill them during mating.
And that idea is one that gets a heart for me
of part of what makes evolutionary biology so interesting,
not the sexual cannibalism piece,
but the idea that things that to us
as human beings are counter-intuitive,
could be predicted by evolutionary biology.
And we can go out and test and see
whether they actually occur in nature.
Now, I read this paper as an undergraduate,
and was really impressed by the fact
that in the end, the mathematical argument
came down to this simple one that you see here.
And that is that you could have the evolution
of such a counter-intuitive mating strategy,
if the expected number of matings in nature for males
who aren't cannibalized was fairly low,
and if males who were cannibalized
had an increase in the number of offspring
that they had as a result.
So the balance then shift in favor of
you're better off mating once and getting more offspring,
rather than having a very small chance
of having a chance to mate again, anyway.
Now, shortly after this paper came out,
it was addressed in a natural history
of popular science article by Stephen Jay Gould.
And for those of you who don't know of Stephen Jay Gould,
he passed away in the early 2000s, but he was and is
an extremely influential evolutionary biologist.
Not just because of his contributions to theory,
but because he also engaged heavily with the public.
He wrote essays in natural history magazines, 300 of them,
over the course of his career,
and he was also a prolific writer of books.
And you see some of his books here.
The wonderful Life,
the book on the upper left is the one that got me hooked
on evolution to begin with.
It's an amazing book if you've never read it.
And a lot of my entree
to understanding evolutionary reasoning
came from Stephen Jay Gould.
He even tackled issues around scientific racism
in the Mismeasure of Man.
Anyway, to get back to cannibalism, Stephen Jay Gould,
this foundational figure for me in evolutionary biology
was not exactly what I would call a Darwinist.
So the idea that I just outlined,
that you could sort of mathematically look at it and say,
"This is counterintuitive,
"but it makes sense in terms of reproductive success.",
that is at the heart of Darwin's idea
about how evolution worked.
But Stephen Jay Gould often quarried whether
that sort of an idea was really going to play out in nature,
or whether evolutionary forces that slow down adaptation
were more likely to be important.
And in the case of this particular paper,
proposing natural selection for sexual cannibalism,
he said, "Do males for the sake of their genetic continuity
"actively elicit or even passively submit
"to the care and feeding of their fertilized eggs
"with their own bodies?
"I find little persuasive evidence for such a phenomenon.
"And I wonder if it exists at all."
I show here diagrams of two of the species
in which cannibalism was fairly well-known,
praying mantis, but also black widow spiders,
which I ended up working on.
To continue with his quote, he says,
"The argument would provide an excellent illustration
"of a curiosity that makes little sense
"unless the evolutionary world
"works for reproductive success of individuals,
"as Darwinism argues."
So, the gauntlet is down,
and this, I wanna say, is where I started in my career.
I'll tell you quickly about the answer to this question,
and move on to tell you where an understanding
of how this works has led to other types of insights.
So when I started working on questions
to do with sexual cannibalism,
that was at the beginning of my career,
I focused on black widow spiders.
And most people are aware of one or two black widows,
types of black widows, depending on where you live.
But I just wanna point out that black widows are
a group of about 30 different species.
They are distributed worldwide.
And if you look at this sort of very truncated phylogeny
or family history that's being worked on
by my student Charmaine Condi,
you can see that they are distributed,
that their phylogeny sort of maps onto biogeography.
And I just wanna point out that a couple of the species
I'll be talking about in depth today,
Latrodectus hasselti, or the red back spider,
and Latrodectus hesperus, or the Western black widow,
are found in Australia and North America.
But there's others that we raise in the lab for experiments.
So you need to to know a bit about their mating
to understand how we can go about testing the idea
about sexual cannibalism.
And spiders mate in a way that are different
from most other creatures.
And that is that males' copulatory organs are paired,
and they're located essentially anteriorly
near the front of their head or cephalothorax.
So this is a closeup of these two structures,
which becomes important later.
These two copulatory organs inseminate
two separate sperm storage organs in females.
So the females' genital opening is located about here
on their underside,
the male, each one of his palps would insert
into one of these sperm storage organs,
and the female can store sperm
for up to two years after mating,
and reproduce successfully throughout that time.
Now for most species in this genus, they mate like this,
these are the black widow mating posture,
a male will climb on the female's abdomen,
males are much smaller than females.
They'll insert one of those palps
the coil that you saw into the female's genital opening,
and then they'll sort of mate kind of belly to belly.
And this is what we see in Western widows.
But in red back spiders, and in brown widow spiders,
one other species in the genus, they do something different.
They start out in the same posture,
but shortly after the commencement of copulation,
the male moves into a headstand posture,
which you're seeing in the video now.
And then he flips over completely,
and he lands with his abdomen with his body
over the female's fangs.
The female will begin to eat him
while he's copulating with her,
and he's able to transfer sperm as he's being cannibalized.
Now, these look, for all intents and purposes,
like males who are adapted
to letting themselves be cannibalized,
the male actively moves into this posture,
other species in the genus don't do it,
and about 65% of matings end with a male being killed
by the female.
So these males seem to be single mating specialists.
This is not random or happenstance.
This is not a male who didn't get away from the female.
This is a male with a behavior that makes it
more likely this will occur.
And so if we go back to this elegant model,
and the Buskirk et al paper,
and we think about these two different things
that might lead to the evolution of a behavior like this,
it turns out that in terms of increase the number
of offspring with cannibalism,
it happens in a slightly
different way than they imagined,
and in a great paper by Kate Barry and colleagues at WASO,
they found that actually, when a male is cannibalized,
his offspring have increased survival and growth
relative to the offspring of male
who's not cannibalized.
So in other words,
the number of surviving offspring would go up.
In my lab group,
we looked at the other side of this and that is the,
sorry, and that there's another way
in which you can increase your fitness.
And that is that the number of offspring fathered
by a male when he's in competition
with other males might also increase with cannibalism.
And that's actually what we found.
Males who are killed by females actually copulate longer
while the females eating them, transfer more sperm,
and when they're in competition
with other males that have mated with that female,
they will father most of the offspring.
So we, thinking about this balance, then,
whether you'd have the evolution
of a self-sacrificial mating behavior,
you then have more surviving offspring
weighing down on the side of
essentially males letting themselves be killed.
But in a series of studies, we also found,
that the balance of that,
the expected number of matings in nature
is actually quite low because most males die
without ever finding a female in red back spiders.
So they just have a very arduous trip
to find females in nature.
They're often killed by predators or die of starvation.
And in fact,
we found that that's true
for other Latrodectus species as well.
So in other studies in my lab,
and the studies in Israel,
they found that other Latrodectus spiders
have the same pattern.
Males have to search for females
through a challenging environment,
and during that mate searching period,
their likelihood of success is low.
But only red backs and brown widows show this balance,
because you have to have both
that there's few mating opportunities
and that you have a benefit from being cannibalized,
in this case, more surviving offspring
to end up with self-sacrificial males.
Nevertheless, this point about high mortality is important
to the what I'm doing now story,
so I'll come back to it later.
Okay, so back to Stephen Jay Gould then,
despite the fact that he debated
whether this type of Darwinian thinking was important
to our understanding of nature,
I would say that in this case,
the evolutionary world does seem to work
for the reproductive success of individuals
as Darwinism argues.
And it's even more compelling
than if it was something
that just made sense to us intuitively, right?
Here's a case where we might not have predicted this
unless we actually worked it out
with theory and then took a look at the numbers.
So since then we found that there's many other species
that also show these kinds of terminal investment patterns.
This is not a one-off in nature,
although it does seem to be concentrated among spiders.
And we find there's common traits of these types of males.
They have very high investment
in a limited number of mating.
And quite often they undergo genital damage
or mutilation during those matings,
and I'll tell you about that later,
they're capital breeders,
which means that they eat only as juveniles,
and they have to accomplish that mating
using only the energy they accumulated
as before they become sexually mature.
Even if they're not cannibalized, they have short lifespans,
and they're all subject to intense sperm competition.
And sperm competition again is when more than one male mates
with a female, especially in a species like spiders,
where they store the sperm, the sperm can be in competition
with each other inside the female's body for access to eggs.
And we showed that cannibalism gives males an edge
in that competition.
Okay, so where am I now?
Started my career with sexual cannibalism
and with being drawn into this debate,
and then once I began to learn more about black widows,
I began to see them as more than just a curiosity,
but instead, a system that it could allow us
to ask some really interesting questions,
because of unique features of their biology,
or I should say extreme features of their biology.
So essentially I was invoking the Krogh Principle,
and recognizing that for a large number of problems,
there'll be some animal of choice
on which it can be most conveniently studied.
In other words, it is not always the case
that the typical laboratory models are the best
for studying every topic.
Even though sometimes we're tempted to do that.
Sometimes there's reasons why a slightly more
unusual model gives you an advantage
and asking a particular question and answering it.
And the question that I was interested in,
how it's going these days is adaptive plasticity.
So let me shift and talk a bit about adaptive plasticity,
and I'm gonna show you how the information we have so far
has brought us, it allowed us to answer a question
that was pressing and where we might go from here.
So this shows you an example of adaptive plasticity.
These are two Daphnia, they are genetically identical.
They are clones of each other.
The one on the left developed in a pond
in which there were cues of predators present.
The one on the right did not.
What happens is that when these are animals are juveniles
if they detect cues of predators,
in this case, chemical cues of predators,
they pour more investment into defensive structures.
And those defensive structures make them
more likely to survive in the environment
in which they live.
The animal on the right not having detected predators
is likely to be maturing
in an environment where there are no predators
and use the resources that would've gone into
building those defensive structures instead for other things
like perhaps gonads, for example,
so they can reproduce at a higher rate.
So there's a mechanistic switch
that allows animals to adapt
to variation in their environment.
And that process is one that is generally interesting,
and for me, very interesting,
with respect to the models that I'm using.
And the reason why I'm interested in plasticity
is to try to understand what happens
when you have an organism that is an adult
that has a fixed set of traits,
and has to accomplish something
in the environment in order to accrue fitness, right?
So the Darwinian currency of evolution.
So let's say for example, in this context,
a male that's maturing in an environment
with a lot of females around,
this relatively large male has high fitness
has relatively, sorry,
low fitness, it's on the low end
of the fitness distribution here,
for reasons I'll talk about later.
But in a different context, perhaps when females are rare,
that same big male may have high fitness.
So males have a set of tools,
their life history and their physiology
and morphology equips them in a certain way as an adult,
and we know from earlier work and from many decades of work
that behavior allows males to take those tools
and adjust to short-term changes
in their environment, right?
So the male may be large,
but he may have strategies or behavioral tactics
to allow him to increase fitness,
even if he's not exactly matched to that environment.
What I'm really interested in with more recent work
is whether it works in the opposite direction as well.
That is when you have an environmental context
that requires a certain type of behavioral strategy
over evolutionary time,
can you have developmental plasticity?
In other words, can that behavioral need,
and I'm just saying that metaphorically,
but can the fact that individuals
with a behavior that matches their environment,
can that feed into the evolutionary process
and cause a shift in life history,
physiology, and morphology,
to give the male different tools as he's maturing.
Let me show you this in a different way.
And this is based on theory on adaptive plasticity
taken from across taxa.
If you don't remember anything else,
this slide will pop up multiple times,
and hopefully you'll remember how this works.
Now, let me start by saying the reason this is important.
So what I'm gonna be talking about is
ways in which you might get adjustments
in individual development, that results in differences
in their adult phenotype that lets them compete, survive,
and be resilient, even under variable adult environments.
Now, the context I'm gonna be talking about
are within the natural range of variation for the species,
but if we understand adaptive plasticity,
which species have it, and when it arises,
it allows us to ask questions about, for example,
which species will be resilient to rapid climate change.
A change in the environment,
can they or can they not buffer that change and survive?
Evolutionary change can take a long time,
but plasticity can happen within a generation.
So let's go back to this model.
So the idea is that you have an organism
in which adult environments vary,
and I'm just gonna call this the adult environment
or the context that is,
under what set of conditions do they have to compete?
If there's reliable developmental information
that provides cues about
what that environmental context is going to be,
then it's possible
that developing juveniles will integrate that information,
change their development in some way
that changes their adult phenotype,
the set of traits they have,
the tools to compete in that environment.
If this is adaptive plasticity, that change,
which was initiated by the detection of some variable aspect
of the environment,
that change will allow these individuals as adults
to compete more successfully
in the environment that they detected,
than if they hadn't changed.
So they're plastic in the sense that it would be
one set of genes that could be switched
in different ways to create different body types
that compete in different ways
depending on what the environment requires.
So it sounds a bit like magic (laughs)
and I kinda think it is,
because it allows populations to be buffered
against short-term changes in the environment.
Now, the context, the environmental changes
or variations I'm interested in is demography
is the sex ratio and density of conspecifics around you.
And I'm really interested in mating behaviors,
and how male reproductive traits, given what they,
the challenges are with respect to
competing with other males
and with convincing females to mate with them,
how those change as population density changes,
and how they may be adaptively plastic.
It's not easy to make rigorous predictions
about what you expect in terms of adaptive plasticity,
because the traits that I'm interested in,
these male reproductive traits
are created by organisms that have to decide
on investment in different types of traits altogether.
So there's a trait you need to reproduce,
like the males' copulatory organs,
like their ability to court a female.
There is an energy and resources
that have to be devoted to development and growth
to get to that point,
to somatic maintenance, the maintenance,
for example of an immune system,
and their trade-offs, because once you use some energy
for developing reproductive traits,
it's no longer available for use
in your immune system, for example.
Now in many organisms,
it's hard to make predictions about what you expect,
in a given environment, in terms of the reproductive traits
that will allow a male to succeed.
And it's hard to predict this because you're constantly
getting replenishment of the resources here
so that trade-off can shift,
and because the number of matings a male can achieve
in his lifetime can continue to accumulate
and happen in very different types of environments.
So a few matings this year or this month,
and a few in the next month,
and the context in which that's happening may shift.
So finally we're back to black widows,
and the Krogh Principle.
So why are these good models for adaptive plasticity?
Because of the fact that their mating system means
that there's a very simplified adult context for males.
They don't eat as adults,
so there's no replenishing of that bolus of resources,
if you will.
They have few or one mating in their lifetime.
Red back spiders, brown widow spiders,
they actually sacrifice themselves to females,
are usually cannibalized,
but even some of those other species
like Western widows, we now know
that their mate search mortality is so high,
that they have a limited number of matings likely
in their lifetime.
So this means you don't really have to think about
trade-offs for future matings.
What you're trying to optimize,
what you're trying to predict,
then that mathematical way is
what would it be best for males
in a relatively tight context around the time
that they become sexually mature
to achieve basically one mating?
The other piece of this puzzle is here, and that is,
you'll only expect to see plasticity
if there's variation in the environment
that affects how male traits will do
in terms of competition.
And if there's something that will allow you
to predict that variation.
Now is the environment variable,
in a way that can't, that could be predictable,
but that isn't just the same
as what your parents experienced?
That's really what we mean by variation.
If the environment is exactly the same
prepared an offspring,
then you don't need to detect things
about the environment, you will inherit from your parents
the traits that will allow you to do best
in that environment, right?
Each one of us sitting here listening
is the product of a successful parent.
So with black widow spiders, we do have that element
of variability that is not predictable based on the parents,
and that's because they disperse
by something called ballooning, as spiderlings.
So on the right, you can see a video from an excellent paper
from a few years ago,
spiderlings let out a little bit of silk,
and this is in early instars, early in their development,
and they essentially fly on the wind to a new habitat.
So where their parents were competing, reproduced,
and where these eggs hatched is not the same
as where the juveniles will have to do well,
if they're going to survive and reproduce themselves.
So the context is definitely variable,
and it's also potentially predictable
because of the fact that males,
as I'll show you soon are very short-lived.
They may live only for a few weeks,
even if they aren't killed by females.
And so that means that the environment that they detect
late in development would be a good predictor
of the adult environment in which they'd have to compete,
but they couldn't get that information from their parents.
In other words, a parent's traits that they passed on,
the static traits won't necessarily allow them
to compete in that new environment.
So let's apply some of these ideas,
and I'll talk to you about these,
this is again, I took a little license here,
and this is a little bit
of a travel log through research over many years in my lab,
ending with things that have been happening most recently.
And it was really applied to this question.
Does adaptive plasticity explain extreme variation
in male size?
So we picked a trait that was particularly prominent,
and that we knew was related to sexual selection,
and we asked whether plasticity
that plasticity framework could help us understand it.
And the variation is quite huge.
So here we see black widows, Western black widows,
and this is a large male and a small male,
45 milligrams versus nine,
which is actually quite a lot of variation,
much more so than you see here
from Manute Bol and Muggsy Bogues.
And if you were in my classroom, I'd ask you to name them.
And one person in the class usually can name them,
unless you're a fan of the eighties,
or lived in the eighties like me.
So extreme variation in male size or weight
is found in a number of different taxa,
and is in itself an interesting question.
So just to show you some of the variation here,
this is from a paper from 2009,
and what they did was calculate the coefficient
of variation for male mass.
So this basically looks at variation
in male mass within a species,
and it normalizes it for the average size of that species.
So in other words,
you can compare a fruit fly to a human being,
and what you're looking at is variation
from some average value.
The gray lines here at the gray bars
are different human populations or societies,
and the black lines are bars are different species,
and this is for 210 different species across taxa.
So you can see there's quite a lot of difference
in coefficient of variation for a male mass,
and as I'll point out again, the Krogh principle
Latrodectus species are very high on this range,
even across species.
So we had seven different species in the lab
help reared under common conditions,
and they range on this upper end of the distribution.
And I love to put this one in
'cause this is the Northern widow,
the Canadian Northern widow populations are right near
the top of this distribution.
So it's an interesting question.
How do you have such wide variation in size
and its extreme, even relative to other species
that show variation in size.
So together with former student Michael Kasumovic,
who's now a professor
at University of New South Wales in Australia,
we started to think about this in terms
of the mathematics of evolutionary change or plasticity.
And what we were interested in the idea
was that there was trade-offs
between the things I show on the slide here
and that the type of context
with respect to population density
in which you find yourself
might affect, which side of this trade off
would be to the highest fitness.
So for invertebrates like spiders,
development time, if you have a given set of resources,
the longer you spend developing, the larger you'll be,
and the higher your body condition.
So the fatter you'll be for each unit length, let's say.
And so this sets up a trade-off,
rapid development would mean that you're smaller,
slower development would mean that you're bigger.
So we were interested in the question
of whether that might tell us something
about variation in size,
and if in fact what we might be seeing
is adaptive plasticity,
where something about population density
affects this trade off.
So let's start with development time,
and ask about what might be affecting the trade-off.
So in work with earlier students, Lindsey Snow
and Emily MacLeod now Dr. Emily MacLeod,
we looked at sperm competition in spiders, right?
So this idea that males were competing for access
to the female's eggs.
And what we found was males actually
in both black widows and red back spiders
lose a part of their copulatory organ,
the genital mutilation, or alteration I mentioned
when they mate.
And that piece, that little tip of their copulatory organ
actually becomes lodged in
the female sperm storage organs at mating.
And in fact, you can find these in museum collections
in 100-year-old females preserved in alcohol.
It's remarkable.
So here we have the red back spiders,
about 73% of the time the plugs,
this tip will be placed in a place
that prevents future males from fertilizing eggs,
and for Western widows, it's fairly similar.
This sets up a situation in which
the first male to mate will father
most of the female's offspring.
So however many males are there in an environment,
when a female becomes sexually mature and receptive,
the first male to get to her
and to be accepted as a mate is
likely to father most of her offspring.
That's what we call scramble competition.
And scramble competition has implications
for development time.
So for a male who's becoming sexually mature
in an environment in which females are nearby,
rapidly developing maybe more important than being large.
So decreased development time in the presence
of females would result potentially in decreased size,
and body condition, because that's how invertebrates work.
Now, what about the other side?
What about size and body condition?
You can't just sort of throw those away and say,
"Okay, well always develop rapidly."
Are there conditions under which increased size
of body condition are important?
And in work with Jeff Stoltz,
we explore this in a variety of different ways,
looking at the outcomes of female choice, competition,
and also what males needed to do
to be successful courting females.
Courtship is actually a really important part
of the mating system of these spiders,
because they spend quite a long time
courting on the females' web,
moving with an energetically expensive vibrational signal,
even before they touch the female.
And then after they climb on the female,
they still spend a long time courting that female, as well.
And in fact, the total time spent in courtship
prior to mating is about three hours for red back spiders,
about one hour on average for Western widows.
So a lot of investment,
especially for a male that's doing this
using only the energy acquired as a juvenile
after a period of mate searching.
Now some great work by Sen Sivalinghem
that I'll let you listen to in a minute,
looks at this courtship pattern.
And -- (loud vibrations)
what you're hearing is actually
the male's courtship vibrations on the web.
(loud vibrations)
Very energetically costly and maintained for hours.
Now when the male gets to the female,
there is potentially competition with other males,
because it's not always just one male.
Sometimes there's two males on the web.
And when that happens,
male size can be important, as well as having the endurance
or the condition that allows them
to get through the courtship in the first place.
And here, what you're seeing is a closeup
of one male who was copulating with a female,
a second male who was actually larger
who bit that first male.
and the first one goes down.
So this sort of competition is a feature
of mating whenever there's two males present
on the web together,
and can result in the death of one of the males.
So it can be very costly.
So in a series of studies and I provide the citations here,
Jeff and I looked at this together
with colleague Daniela Liaz, Andrew Mason, and Paul DeLuca.
And we asked the question across these studies,
can size predict who wins, and in fact it can.
It's about 75% of the time the large male wins,
about 25% of the time the small male wins.
So there's an advantage to being large.
Larger males can endure that long courtship,
they can endure a long mate search
and they also do better in direct competition.
So if you look at the flip side of this trade-off then,
endurance and direct competition
favor larger size and or body condition,
and so if you're in a context
in which size and body condition are important,
in which there's likely to be a lot of competition,
in which you have to search a long distance
to find a female,
then body size and condition would allow males to do better.
And the result is that their development time
would have to be longer
at a given level of resources to build that type of a body.
So Mike then developed this predictive framework and said,
"If this is true, if what we understand so far is true,
"if plasticity works the way that we expect,
"then what we should see is that at high densities,
"at high population densities,
"when females are close by and present in large numbers,
"males should decrease the development time,
"at the cost of smaller body size and body condition."
When there's very few females,
when there's a low density population
or females are far away,
males should increase their development time
in order to increase body size and condition
and do well under those contexts.
Now I'm using verbal shorthand in evolutionary terms
what this means is any male that had a plastic response
to detecting something about population density
and made this trade off longer or shorter development times
would be favored, and that trait's expected to spread
through the population.
So if we go back to this framework then,
what we expected then is that low density
males would be adapted to endure,
to develop for longer and be larger,
at high densities, they'd be adapted to scramble,
and they would accelerate their development,
be smaller but be better able to compete
and they rapidly rapidly get to females.
So what's missing now is
what about their environment would provide cues
about which of these strategies they should take.
And we knew something about this
for both red backs and black widow spiders,
and part of that is dependent on their lifespan.
So red back spider males,
even when they're not killed by females
survive for only about 25 days,
that's under optimal laboratory environments.
Typically we expect in the field,
they actually survive for only a couple of weeks.
In contrast, Western black widow males
are much more long-lived,
they will live for about three months,
which is typically the duration
of a complete mating season.
In both cases, males become sexually mature
at various times through the season.
So for red backs, there's a narrow window
around the time at which they become mature,
and under which they have to compete,
for Western widows, they tend to be competing
across an entire chunk of a season,
during which the demographic context may change.
What might they be using to detect this?
In both species, they have access to sex pheromones.
Females produce sex pheromones that are released
into the air and that males can detect at a distance.
They also have pheromones that trigger courtship
when they're in contact.
We know from previous work
and some of this with Luciana Baruffaldi,
some with Catherine Scott,
some with Jeff Stoltz, all three of them now doctors.
Congratulations (chuckles).
We know that sex pheromones indicate
the receptivity level of females,
and it also can give the males information
about the risk of cannibalism, but that's another story.
So some of the ways that we look at this
is by looking at male attraction
to pheromone-laden filter paper,
either in a setup like this and an airborne pheromone trial
or in contact.
So information in the air
could give males information about density.
And we expected that would be important
for red back spiders in particular,
because what they smell as they're developing
in that last instar will be very relevant
to how they have to compete
in the few weeks during which they would survive.
So fine-scale variation, local variation,
both temporal and spatial would be important.
We didn't expect the same for black widows,
and that's because they live for an entire mating season,
which may be three months in duration.
But as I'll show you in a minute,
we did know that density of females is predictable
in a seasonal pattern in black widows,
over the course of those three month periods.
So what we expected then
for black widows is that they would use cues
of the time of season to determine plasticity if it existed.
So we did field work that showed this.
This is work with Catherine Scott and Sean McCann and
I should say, thanks very much to the Tsawout First Nation,
for giving us access to their lands.
And over the course of the season,
what we found is that at the early in the season,
females are present at fairly low densities.
That shows you the number of females
from July through September at this field site,
and the number of males,
and you can see that as the season goes along,
more and more females become sexually adults,
and become receptive,
so that there's a higher density
of females towards the end of the season.
Similar work in the Hastings Natural History Reserve
in California showed the same sort of pattern
in that early in the season in the fall,
over the course of three months,
females tend to be present in high density,
many of them unmated.
Later in the season,
females are unmated and present at low density.
So we have this situation
in which we do have this difference,
and we have two different types of the cues
that could demonstrate what's going on.
So in the lab, we did an experiment,
a series of experiments, really, where we expose males
to pheromones, red back males to pheromones
produced by females at simulated high or low densities,
and we found just what we predicted.
When we simulated low density of females,
males slowed down their development.
Their longevity was higher
and they were larger as a result.
Whereas when lots of females could be detected by males,
they developed fairly rapidly, at small size.
We did similar experiments with black widows,
but in this case,
simulating differences in this time of season,
and what we did was simulated,
I skipped that one,
we simulated the fall typical
or spring typical temperatures,
when we expected males to evolve,
to develop to endure long distance, searching
for mates versus having lots of females around
as we showed in the field data.
And what we found was,
as we predicted when males were reared under conditions
typical of a high density population,
that is typical of a fall,
they developed much more rapidly,
and as a result, they were smaller
than when we did the same
in the spring typical temperatures.
More than that, we asked about
whether they were adapted for scramble competition,
by essentially racing them on a track.
(chuckles) This is something we do with widow spiders.
We simulate a predation stimulus
by lightly touching them with a paintbrush,
and then we see how fast and sustainably they run.
The more sustainably they run,
we refer as the better they'll be at scramble competition
performance racing to find a female.
So I'm just gonna show you some of the data
from a number of times amount stops in this condition.
So males who are able to run continuously
with fewer stops are better at scramble competition.
And what you can see here is
that males reared under fall typical temperatures,
which simulate the time
during which should be a lot of females available,
they rarely stop,
regardless of the diet in which we reared them.
Whereas males reared on spring typical temperatures
are only able to run sustainably
if they have a very high diet.
So males on a lower diet
show this big difference in that they're stopping
all the time.
More than that,
we showed in another set of experiments,
that if you release males in nature,
or if you put out traps that draw males in
by using pheromones of females,
and then take a look at the size of males
who show up at these traps,
the timing is very different,
as a function of male size.
We measured a measure of fitness,
which looks partly at how quickly males
reach these pheromone sources,
and what we find that is it's actually
the smaller males who get there faster.
So essentially then we've made our way
through this theoretical framework,
we've used a species that according to the Krogh's Principle
may be a really good one for looking at adaptive plasticity.
And we now have evidence
that not only the adult environment changes
with respect to the density and availability of females,
not only that for some that species are able to detect
that difference either through pheromones
or the time of season,
and they changed their,
that they changed their development as a result,
but that changed developmental pattern
can also lead to a fitness advantage
in the environment in which they develop.
I wanna stop there so that we have time for questions.
And just wanna say that we are exploring
many other areas in the lab,
this is the one that I love talking about,
because it is to me, such a great example
of why even though there are weird
black widows with cannibalism,
they may tell us something fundamental about theory.
And I really wanna thank these undergrads.
I like to talk while they're up on the screen
because this work requires
that we rear thousands and thousands of spiders,
and I have 10 to 15 undergrads
in a non-COVID year working in a lab at a time,
and I wanna thank them.
Ariela is named in particular,
and so Sean on the next slide,
because they are my COVID-rearing crew,
and they are working even while my lab was shut down
as a essential worker, so thank you for that.
And then finally,
I really wanna thank all the lab members currently
who are instrumental to everything I do.
And I neglected to say on the first slide,
although I did include his Twitter handle,
Dr. Sean McCann took the outstanding
many of the outstanding videos
and pictures you saw in this presentation,
and they're amazing, thank you, Sean.
And then finally, I think I'll stop with that
and just say thanks also to the million black widows
we estimate we've reared
in the lab over the last 20 years.
And I thank you for your attention,
I'm happy to take questions.
- Thank you so much, Maydianne,
that was a great talk,
the research is really interesting.
We have a bunch of questions here.
I'll start with this one.
"If the male black widow has a lower survival rate,
"does this affect the ratio of male to female eggs
that are produced?
"Would there be a higher percentage
"of male spider eggs laid by the female?"
- Outstanding question.
And I would that I had an answer already,
because I'm asked that question frequently.
We don't know yet.
As far as we can tell, the sex ratios are usually 50-50
when females produce offspring,
but we know from other species
that when there is different payoffs
for having males or females,
that they can adjust the sex ratio of their offspring.
So there's some classic studies in birds,
there's one species of spider where they're able to do this.
And we know they can do that
in various kinds of really fascinating mechanistic ways.
The question would be, what's the advantage
to the female of having more males or females,
rather than kinda what's the sex ratio at the end.
So if females are able to manipulate the sex ratio,
I predict we probably wouldn't see it in the lab
because they're not getting the cues
unless we do an experiment of a higher low density,
or a situation in which having a male
would be particularly valuable or particularly costly.
So what we really need to do is figure out in the field,
does a female who skews her offspring towards males
end up with more grand offspring than one who doesn't,
and then we would simulate those conditions
and ask if they shift the sex ratio.
My postdoc, Luciana Baruffaldi's actually taken
with those questions right now.
So invite me back next year,
and maybe I can tell you the answer.
- Wonderful talk.
Thank you so much. - Thank you.
I'm gonna go sort of in order,
why do female black widows eat their mate?
You sort of alluded to that, but --
- Yeah. - There's a direct question.
- That's a great question.
So we do know that from that one study
that came out of Australia, actually,
Kate Barry's lab, Sean Wilder,
and I'm sorry, Boiso, I forgot your first name,
Luke, I believe,
that there is an advantage for females
through cannibalism in the sense that their offspring
is not that they have more offspring,
but the offspring actually developed faster,
and have higher fitness for that reason.
What we don't know is whether that's because
of something specific in the male's body,
or whether the female is actually allocating more resources
to males, to offspring after she kills her mate.
Now that sounds weird, but we know that cannibalism
seems to be a mechanism of choice for females, in a sense,
and so it could be that females are selecting males
who are cannibalized by females
are better quality males in some way,
and so the female invests more in their offspring.
But the truth is we don't know.
And one of the reasons we don't know is that
unlike the three weeks to a month for a male to live,
females can live up to two years.
And so we are just now starting to accumulate enough data
to ask these questions about female strategies
instead of focusing all the time on the male strategies.
And I'll be excited again, sorry to tell you,
maybe in a couple of years,
what the answer to that question is. (laughs)
- Maydianne, I'm gonna ask two questions,
'cause they're related.
Are there, in a population,
are there more males than females, generally?
And if it's so hard for males to find a female,
you know, how often do they need to compete
for the same female,
and do the males often run into each other?
- Great.
So this is a species with overlapping generations
that overwinters at multiple life history stages.
So that's the jargon side.
The last jargon side is,
males are maturing continuously through the season.
Females are as well, but really only one cohort of them,
so one set, it takes them a long time to mature.
So what that means effectively is that
even if the sex ratio in each egg sac is 50-50,
we have males for multiple egg sacs
over the course of the season maturing,
during the time that only one set of females are maturing.
So the questions about sex ratio
actually become quite complex.
Even though males are dying at high rates
before they reach females' webs,
there's multiple cohorts maturing.
And what you end up finding is
that the sex ratios are actually skewed
towards males for a big chunk of the season,
because they mature so quickly.
And so you do find really frequently
that there's multiple males on females' webs, up to eight,
but on average in the systems I've studied, about two,
and in the black widows we found,
it's common to find at least two or three as well.
So there's lot of competition.
- The next question I'm gonna ask is,
have you identified the range
in which males can be plastic in their development?
I imagine there's a point in the embryonic development
where plasticity is not possible
independent of the environmental cues.
- Yes.
So you're right.
That window for plasticity is actually
a critical part of the equation that I kind of glossed over.
We do predict that it would be only in the last instar.
So males of invertebrates go through
multiple instars of growth,
and this species they shed their skin,
they grow a bit, they shed their skin, they grow a bit.
Males of red backs, it's usually five or six instars
or growth stages before they're sexually mature.
We've done all these experiments exposing males
only during their final instar,
during that final growth period.
And the reason for that is A, it's easier, (laughs),
but the main reason is
we, because females are becoming sexually mature
and getting mated at a regular rate through the season,
if you wanna predict in evolutionary terms,
males who pay attention to those pheromones
only during the last instar
will probably do better than males
that try to integrate the information
across their entire development,
because the situation's changing.
And what we're expecting is
that it's the cues that predict what's gonna happen
when the male becomes sexually mature,
i. e. within a week or two
of detecting it that make the difference.
So the shifts we're talking about are really on the order
of only a few days, but that time is enough
to allow that male to get to the female,
mate her, plug her, and make her unavailable for other males
before another male who took longer to develop.
- The next question is regarding the hypothesis
that environmental cuing comes from pheromones,
do you have any strains
in which females are incapable of producing pheromones
where you could test that more specifically?
- So the pheromone question is fairly well-established.
We, so I should have said in more detail
that experiment involved caging males
in screen cages with females
and screen cages surrounding them.
These spiders don't see, their vision is poor.
They can see sort of light and dark,
but they don't really see images.
So there's no visual cues.
They were isolated for vibrational cues, as well.
So the only cues reaching the males
in those contexts were actually
the airborne pheromones coming out of the web.
In addition to that,
in the field what we can do is get a female to create a web
inside a screen cage, take the female out,
and then you put that cage in the field and males show up.
In fact, the first time we were working on Northern widows,
we weren't sure if we were in a field
with a lot of spiders, and we had to carry a bag full
for our field work
of these screen cages that had no females in them,
just the silk, and the males were coming,
as we were going out, trying to put the cages down.
So there, it's quite remarkable,
and well-established that the pheromone key was there.
And in that experiment for development,
that was the only cue available to male,
the different males that differ
between the two experimental contexts.
- The next question I'm gonna ask
is a compilation of several.
One is, how many offspring can a spider have?
And there've been several people,
why is it that male widows have a shorter life span
than female widows,
even without being eaten by a female?
- So how many offspring can they have?
Females can produce,
depending on the species of black widow,
100 to 400 eggs per egg sac,
that all hatch into spiderlings.
And they can do that once every two weeks,
if they're well-fed for two years.
So I won't do the calculus on the fly,
but it's a lot of offspring.
That's also why some of these species are invasive.
So if you have one mated female showing up someplace,
they can churn out thousands and thousands of babies.
Now, the other question was, why this difference?
So that's a whole another set of questions.
I love that.
Thank you for that question.
So these species are extremely sexually dimorphic.
Sexual dimorphism of this type, sexual size dimorphism,
when you say very large females,
and very small males are the subject
of a whole another field of study.
You see that in other species as well,
but it reaches, I think its Zenith probably
in spiders, and essentially they're adapted
for different types of life history.
So some people call males sperm on legs,
partly because the fact that you have scramble competition
and that males who get there earlier will do better.
Males have not evolved to spend the long time
having huge body size.
Females on the other hand,
their body size is tightly correlated
with how many eggs they can produce.
So in terms of evolutionary fitness or Darwinian fitness,
females who are able to be grow to be large enough as adults
sufficiently large to produce more eggs
will do better than females that let's say
had shorter life history.
So in terms of the evolution of these life history patterns
how much time you spend developing
when you become sexually mature,
how many offspring you can produce,
males and females are just radically different.
And in fact, sorry, I'm gonna go say one more thing,
in the early literature,
they didn't know the males were the same species.
There's really early literature on spiders
where like "There's this big spider,
"then there's all these little things
"hanging around on web."
And they weren't sure at first it was the same species,
those are some great early work that says
yeah, in fact, those are the males.
- I'm gonna double up on the next question, as well.
Does cannibalistic behavior occur
in invertebrates outside of the arthropods,
and then can you describe the process
of capturing the spiders and how the traps work?
- Yeah.
So does sexual cannibalism occur
outside of insects and spiders?
(laughs)
Not in this form.
There's the odd anecdotal report in other groups,
there is a similar sort of bifurcation or shift difference
between male and female in some other species.
So one of the classic examples I often talk about
is a little marsupial mouse, a little mammal,
that Australians endearingly called dibblers,
but they're actually called Apicalis, I guess,
is the Latin name,
in this species there's no sexual cannibalism,
but in terms of one thing being
males being evolved for short lifespans
and females for relatively long lifespans,
the males of these species mate
in over the course of one season only,
whereas females can survive for more than one season.
And during that season, the males actually engage
in such pitched competition because of sperm competition,
that they shift all their resources into producing sperm
into competing for females,
their hair drops out,
they're riddled with parasites,
because they shift energy away from their immune system,
and they die at the end of the season,
whereas females are longer lived.
So it's not exactly the same,
but this idea of investment, differential investment
is seen elsewhere.
And then I forgot the other question,
'cause now I'm thinking of these poor little marsupials.
(laughs)
- Yeah, do fields capture --
- Oh yeah.
- That's where for the spiders.
- If I'd had a wee bit more time,
sometimes I just show like five slides on the stuff we do
in my lab 'cause people are always like
"How do you work on spiders?"
So females can go into these screen cages,
the silk that they produce is laden with pheromones
and produces airborne pheromones,
so again, we can make basically a pheromone trap for males
by just having females build dense webbing
inside a screen box,
putting that box out in the field.
You can then, in our first round of doing this,
we actually used sticky traps around those dense boxes
so when males are drawn
and they were stuck to the traps,
and we could measure them and things,
we felt terrible,
'cause a lot of the males died,
and it turns out that if you don't have the traps,
Sheena Fry, my student discovered this,
the males would climb on the cage and just sit there,
like, "Where is my female?"
(laughs)
So you could actually just pluck them off,
and go regularly and collect them that way.
We can also and we do mark female webs
in the field because females are sedentary.
They typically don't move once they're sexually mature.
Even before that.
And then we can mark females and males
with paint colors on their legs,
so when we're doing these actives surveys of male movements,
we all collect males, take them to the lab, weigh them,
take pictures so we can measure them,
and use tiny drops of paint on their eight legs
by four or five different colors,
gives you a lot of different you know, right leg blue,
left leg, white, whatever codes.
And so we know males, not by name, but by their paint codes.
And so if we find them later on
in another females web, we'll know,
okay, this male move from web number five,
which has been there for three months
and has a female who's immature,
and moved to this female, who just became sexually mature,
and they moved this distance, et cetera.
- And I would like to end with this question if we may,
and this is from a friend of,
or a person from the English Department
at University of Waterloo, just to --
- Oh, hi.
So -- - Hello, Canadian.
(laughter)
Do you have any suggestions for getting kids of color,
especially in developing countries
interested in the area of evolution?
- Yeah, I think it depends on understanding
what's interesting to them in their context, right?
And in fact, I'll just put in a plug right now
for Black and Entomology, Black and ento,
we're gonna have a week at the end of the month,
we actually talk a lot about the fact that
there's a lot of cultural knowledge
in places where people tend to be a little bit more in touch
with their environment than we are.
And that as Western scientists,
as, or developed global North scientists,
we tend to go into these places
and tell them what's interesting to study.
But if instead we ask what is already there
that they're interested in,
there will be evolution stories in it, right?
So it's a challenge, but check out Black and Entomology,
'cause entomology's one way to get them into it.
They're cheap to work on,
they're plentiful.
You can do observational and experimental work,
and they are great models for evolution.
So thanks for ending with that.
- So I'll turn it over to my colleague, Dr. Burchsted.
- That was absolutely fascinating.
I can't thank you enough for being here,
and clearly stimulating our audience with lots of questions,
and lots of information and lots of evolutionary thinking.
So thank you, Dr. Andrade for coming
to give our founders' lecture
at this 42nd Annual Darwin Festival.
- Thank you for inviting me.
- I second that, and this ends our presentation for today.
I wanna encourage folks to come
to subsequent talks for the Darwin Festival.
The next one will be at 11 o'clock tomorrow.
Thanks so much.
Bye-bye.