eLife Episode 52: Fossil Flowers, and Fur Seal Parasites

19 December 2018
Presented by Chris Smith.

In this episode of the eLife Podcast, the nerves with a taste for salt, why fur seal pups succumb to hookworms, the oldest fossilised flowers ever found, the monkey business of chimp personalities, and the 11 million year old flying squirrel foung in a rubbish tip...

In this episode

Drosophila labellum with a novel class of salt-aversive neurons labeled.

00:34 - How flies taste salt

Why sodium can taste both good and bad to a fruit fly...

How flies taste salt
with Mike Gordon, University of British Columbia

Salt is one of those things that take too little and you’re dead, but too much will kill you. So animals have evolved very complex mechanisms to taste salt and control how much they eat, and that includes fruit flies. And what Mike Gordon has found is that flies have multiple salt-detecting nerve cells; some of these respond chiefly to low concentrations of salt in the diet and seem to encourage intake. The others respond to high concentrations and normally deter a fly from eating a foodstuff that might contain a toxic salt burden. But, as Mike explains to Chris Smith, the intriguing thing is that, if the animal is deficient in salt, it can temporarily override and ignore the aversive “toxic” signal…

Mike - Well we really set out to try to understand how the taste system of the fly interprets salt in their environment, because salt is a particularly interesting taste modality because it's attractive at low concentrations but it's actually aversive at high concentrations. And so, unlike most tastes, which elicit either attraction or avoidance, salt actually does both. And so we figured that the way that the taste system must interpret salt had to be more complicated than other tastes.

Chris - Is it complicated like that because you need a bit of salt, but too much is a bad thing?

Mike - Right. Exactly. There were models in the taste field that suggested that there are essentially two different responses that get layered on top of each other. So there's an attractive response that kicks in at low concentrations and then, as you get to higher concentrations, you'll get an aversive response that sort of overrides that. But what we found is that it's actually even more complicated than that, and there's actually two populations of cells that are attractive, and respond at low concentrations, and two distinct populations of cells that are aversive and respond at high concentrations.

Chris - And this sensation or this detection this is happening in the equivalent of a taste bud?

Mike - So flies are a little bit different than us; their taste system actually uses neurons to detect tastes. And so these neurons, that express the receptors that actually bind to the taste ligands, are in various body parts of the fly. They're present on the mouth of the fly. They're actually also present on the legs of the fly, which makes some sense because flies spend a fair amount of their time actually walking on their food! And so it's a good way of kind of deciding what the food tastes like before you actually start eating it!

Chris - The mind boggles of what would happen if we could do that! But how did you actually do the experiments, because if you want to unpick what's going on how did you actually put a label on what the different nerve cells are that normally detect things, and how they are individually then responding to salt, or not?

Mike - So what we started with was trying to make a fairly comprehensive map of the taste system using different markers. These are just genetic markers based on the expression of specific receptors. So, for example, a receptor that responds to sweet compounds, if we use the gene that encodes that receptor then we can label the neurons that respond to sweet. And so we did this, and compared them all against each other to try to make a map where we had different, discrete populations that we could then look at the activity out of.

Chris - I get it. So you've got a molecular label if you like - a chemical tag - that says "I am this sort of nerve cell with this sort of receptor on me," and you can then test how that particular class of receptor responds to salt and at what concentration?

Mike - Exactly. And so to do that what we actually do is to express another label in those particular neurons. And this particular fluorescent protein will actually become brighter when the neuron fires, and then we use a microscope to just look at the activity of these neurons while the fly is tasting different concentrations of salt.

Chris - But just to be clear: under all circumstances - even when there is an aversion to salt at high concentration - it's still activating those cells. It's just that, centrally, that's interpreted as "that's not very nice" versus when the same signal - the excitation - comes in from a different class of nerve cells it's interpreted as "yummy, that's nice, I like that".

Mike - Exactly. And so what actually happens is that those "yum" cells actually continue to fire even when the salt becomes a high enough concentration that it's aversive, but it's just that the "yuck" cells kick in on top of that and override the attraction of those other cells.

Chris - So that sort of aligned with what people had decided probably was going on previously. So where does the extra detail come in which you flushed out with the new way of unpicking what these different receptor classes are?

Mike - So there were two main things that we found. One is that we identified the second population of attractive neurons, which had not really been found or characterized before. But the potentially more interesting thing that we found is that the second population of aversive cells - the negative cells - had a really interesting characteristic, which is that the fly only paid attention to the activity of these cells when it had previously eaten salt. So, if the fly became deprived of salt, they then ignored the sort of bad signal coming from these cells, presumably because when you're salt deprived, even a little bit of a high concentration of salt is going to be beneficial.

Chris - That's intriguing isn't it. Where do you think that decoding is happening is that a central process then so that the fly brain is comparing how much salt it knows it's got on board as total body sodium, for example, and it's saying "well, I'm going to disregard this aversive input because I can tell that actually my salt reserves are very low across my whole body".

Mike - We think it must be, because we actually then used optogenetics, which is a method to essentially activate neurons using light, and we activated these different populations of neurons. And so, even when we force the activity of these negative neurons, if the fly had been deprived of salt, they didn't care about the activity from these neurons. So it can't be happening at the sensory neuron level - it must be something downstream. So we presume that in the higher order circuits of the fly brain that this is integrated somehow...

Patagonian fur seal pup

07:09 - Fur seal pups and hookworms

Sea temperatures affect plankton growth, which in turns alters fish abundance. So warm seas force nursing seals to spend longer foraging and less time nurturing their pups...

Fur seal pups and hookworms
with Mauricio Seguel, University of Georgia

In this interview we’re off to Patagonia, where veterinary pathologist Mauricio Seguel explains to Chris Smith how he has discovered that climate change, by forcing their mothers to spend longer at sea foraging, is making fur seal pups much more susceptible to parasitic hookworms...

Mauricio - Fur seals live between land and the ocean; so they find their food in the ocean - mostly fish - but they reproduce on land, so they need a good piece of land where they can mate, give birth, and then take care of those pups for about one year. Usually they stay with a pup for one or two days, and they they go to the ocean to find food, produce more milk during that trip, and then two, three days later they come back to the mainland where they nurse their pup for another one or two days; and then they go back to the ocean to find food again, and again...

Chris - And what was the question you were specifically trying to find out about that life cycle?

Mauricio - So in this population, we saw that there is a significant amount of mortality in the young animals - in the pups - because of a parasite disease - a nematode, like a worm -that lives in the intestines of the pups and it sucks the blood of these animals causing disease and mortality.

Chris - And on what sort of scale do you see mortality because of this?

Mauricio - In some years it could be up to 25 percent of the pups that are born.

Chris - That's a very significant proportion isn't it! Tell us about the lifecycle of the parasite itself. What does it do how does it spread and how does it cause disease.

Mauricio - This is a very unique parasite. The way the parasite reach these pups is only through the milk of their mothers. The very first milk that their mothers give these pups get the larval stages of these worms. These worms goes go to the intestine where they mature and they start releasing eggs; these eggs reach the environment where the larval stages remain for a little bit in the soil, and then these larvae, which are very little, they are worms and can penetrate the skin; then these larvae they just remain in the subcutaneous tissues in the blubber of these animals. But if the animal that got infected through the skin is a female, when this female gets pregnant, these larvae sense somehow that this female is pregnant and they migrate to the mammary gland; and in the mammary gland they migrate through the milk to get transmitted to the pup again.

Chris - So what did you actually do to study how the parasite is imposing a burden on the first population?

Mauricio - The first thing that we did was to measure the mortality and to try to understand, well, what's driving this mortality? So we first saw that there were pups that they were able to fight this infection by creating a very strong immune response against this worm; but we saw that other animals were not able to fight this infection and they ended up dying.

Chris - Is that death owing to the fact that the animals are just susceptible for some reason - genetics for instance - or is there some other reason that they're more susceptible than other animals?

Mauricio - That was one of the main questions of our study and we saw that most of the explanation of why some animals cannot fight infection is driven by the care that they get from their mothers. So the animals that spend more time with their mothers tend to have a better immune response and they can fight these infection better and they survive.

Chris - That sounds logical; but what determines why some of them get more maternal input than others?

Mauricio - So, the mothers can spend more time with their pups when the conditions in the ocean are better. So when the conditions are good and there is a lot of fish in the ocean, these females they can easily find food in the ocean so they return very early to nurse their pups. However, when the conditions and the ocean are not that good and there is less fish and these females cannot find food that easily, they tend to leave their pups alone for a longer period of time.

Chris - So putting that together then, when you've got less plentiful food in the ocean - for a variety of reasons - the mothers are forced to make more frequent and longer forays out fishing to feed themselves. So, therefore, the pups are not getting the same input from their mother in terms of milk and therefore energy. So they're being deprived of food for longer, and that makes them more susceptible to succumbing to the parasite?

Mauricio - Yes, exactly. Additionally, we saw that this link is mostly given by the energy balance of the pup. So these pups that spend more time with their mothers, they potentially receive more milk because they tend to have a better energy balance: they have higher levels of blood sugar, blood fatty acids that are very important for the body of these pups to have enough energy to devote to the immune system.

Chris - Again that's logical isn't it that there should be that relationship; but what are the factors that you refer to that affect how plentiful the fishing is for the females and therefore how long they're forced to spend away from their pups or not?

Mauricio - There is this link between the temperature of the ocean and the flow of nutrients for phytoplankton and zooplankton. So these cycles are driven by temperature mostly, and by winds in the ocean. Basically they dictate what is the productivity, or how much life there is, in certain period of time in a particular zone of the ocean. We saw that in this place where we were doing the study, in the Northern Pacific Patagonia, when the temperature of the ocean is too warm there tends to be lower productivity. So there is lower concentration of, for instance, phytoplankton. We saw that, during these years, the fur seal females spend more time in the ocean trying to find food.

Chris - So, if warmer temperatures mean fewer fish and that means hungry females and therefore hungrier pups, what might be the implications of climate change then?

Mauricio - The implications of climate change are big in this case. So the temperature in the ocean is impacting the health of these first seal pups and their survival. Not directly, because they don't swim; they don't go to the ocean, but through their mothers; their mothers are feeling this effect and, even though it's not killing their mothers, it's affecting how much energy these mothers can transfer to their pups and this affects the chances of survival of these pups...

This is a Nanjinganthus fossil, showing its ovary (bottom centre), sepals and petals (on the sides) and a tree-shaped top.

13:59 - The oldest fossil flower

Fossil remains of flowers dating back nearly 200 million years have been uncovered by palaeontologists in northeastern China...

The oldest fossil flower
with Xin Wang, Nanjing Institute of Geology and Palaeontology

The textbooks tell us that flowers first appeared about 125 million years ago. But now a dig in northeastern China has turned up literally hundreds of fossil flower specimens. The structures of the flowers show that they’re from a group of plants called angiosperms - these are the common vascular, seed-bearing plants we see around today. But what’s extraordinary about these newly-found flowers is that they date from nearly 200 million years ago - proving flowers have been around for much longer than we first thought. Speaking with Chris Smith, Xin Wang made the discovery…

Xin - About two years ago we discovered many many specimens of a flower from the early Jurassic. Just in the suburb of Nanjing City. Early Jurassic means 174 million years before today.

Chris -  So these are very ancient specimens! How do they fit into the timeline of what we understand about the evolution of flowering plants?

Xin - The mainstream idea about the evolution of flowers is that flowers only existed since 125 million years before. But our discovery is far far beyond the scope. And we have so many specimens we are very confident with our conclusion. They are angiosperms, and the flowers in the early Jurassic.

Chris -  Could you describe what these particular flowers would have looked like for us?

Xin - Each flower is about a 13 millimetres in diameter. It's a very small flower.

Chris -  And you say that these are angiosperm flowers? Why is that important?

Xin - Because in the textbooks people were taught there was no angiosperms, no flowers in the Jurassic; which means we have been misunderstanding the history of a flower and angiosperms.

Chris -  And how did you make the discovery of these flowers - where did you find them, and in what sort of context?

Xin - Well the situation is there are many discoveries of early angiosperms in China; formally it's in the northeast China. My previous work also focused on the northeast. And we somehow just ignored something nearby! About two years before, one of my colleagues, Dr Fu, found the first sign of flower in the suburb of Nanjing. And then we went there together. We were so lucky that in the first half day we'd got more than 200 flowers, and sometimes a single piece of rock there are almost 80 flowers!

Chris -  Why do you think these flowers are so well preserved and why are there so many of them where you discovered them?

Xin - The flowers are preserved in a different states and orientations. Because the huge number of specimens, it gave us a chance to observe the flower from different angle and perspectives, and the presentation is not always the same. Some of them we can see the internal structure. Some we don't. So, if we combine all that information from more than 200 flowers, we can reconstruct a single flower, which is what we did in the paper. And why the flowers are concentrated in this area is because the flower probably flourished in this small area, probably very close to water, and they didn't grow too much in a forest, or somewhere else. So, when they're preserved in some kind of lake or pond they are just buried there. 

Chris - What do you think these flowers turned into?  Can you see, or can you trace any further lineage or timeline from these flowers onwards in history? 

Xin - Honestly, we have no information about this yet. We're know nothing earlier oe nothing later than this.

Chris -  So, at the moment, we know that these flowers come from 175 million years ago or so, pushing back the date of the first flower by more than 50 million years. But, obviously, that doesn't mean that that's the precise moment when the flowers did first appear. So that means that the first flowers are even older than this doesn't it?

Xin - Yes definitely! And flower's history must be much older than this.

Chris -  And in terms of what must have been going on in parallel, does this give us some insights into what animals were doing at the same time as the plants were evolving these flowers?

Xin - Current information about this flower doesn't suggest there were insects or animals involved in the pollination of the flowers. They have a dendroid form, which means it has an increased receptive area of the stigma, which is frequently seen in flowering plants which are pollinated by a wind rather than by insects...

Different personality traits are linked to different lifespans in male and female chimpanzees.

19:25 - Chimpanzee personalities

How do the personalities of chimpanzees affect their prospects for reproducing and longevity?

Chimpanzee personalities
with Drew Altschul, University of Edinburgh

The phrase “go ape” means to become very angry or get very excited; it’s probably also a lot more accurate than its inventors realised, because we inherited our personality traits from the great ape ancestors that we share with chimpanzees; and that means that chimps have them too. And they’re under evolutionary selective pressure: a favourable trait will mean you live and reproduce more. Drew Altschul, at the University of Edinburgh, has been looking at which ones really matter to chimps…

Drew - So we wanted to understand the evolution of personality, both in humans and in our closest relative, which was chimpanzees. Humans have five main personality dimensions, which are agreeableness, extroversion, conscientiousness, neuroticism, and openness; and chimpanzees share these same five dimensions, plus they have a dominance dimension. We believe that there is an ancestor of humans and chimpanzees that shares these dimensions. And so, by understanding how chimpanzee personality relates to chimpanzee longevity, we can understand one aspect of how natural selection is shaping the development of personality.

Chris - So how might you predict it will? What sorts of personality traits - before you you've gone anywhere near any results in this study - what went through your mind in terms of what will be related to what?

Drew -  There's information coming from the human literature as well as the animal literature. So, in humans, high neuroticism and low conscientiousness tend to result in increased mortality. So if you're more neurotic you tend not to live as long; if you're more conscientious, you tend to live longer. Whereas, in animals, it tends to be more of a focus on social traits; so more extroverted individuals to live longer; more dominant individuals tend not to live as long; and, to a lesser extent, the more agreeable individuals live longer as well.

Chris - So that's what you're sort of expecting to see. How did you therefore do the study?

Drew - We used a questionnaire that's been validated across many years. We basically asked people who know the chimpanzees really well - those are keepers and researchers and other staff - to rate them. And by bringing together multiple questionnaires where everyone has filled out the same items we can basically add these items up and use our predefined structure to come up with a bunch of scores one for each personality dimension. 

Chris - How many animals did you consider? 

Drew - We had 538 in the final analysis.

Chris - Was that males and females?

Drew - Yes, both males and females.

Chris - And when you pull all the data together just in broad terms first of all what were the findings?

Drew - We found that male chimpanzees who were more agreeable tended to live longer, and more open females also tend to live longer. But we didn't find any associations for any of the other personality dimensions.

Chris - That's interesting isn't it; why do you think you saw that effect for the males in terms of getting on well with other males but you didn't see it for the females, because these are social animals are they - they hang around in big groups?

Drew - Yes they are. Agreeableness is one aspect of sociality, and among the males agreeableness is essentially the opposite of aggression and there's evidence to show that more aggressive individuals - particularly males - tend to live less long. And so what's possibly happening is that the more agreeable chimpanzees are better at forming coalitions and making it through tumultuous social circumstances and end up living longer because they end up in basically fewer harmful circumstances.

Chris - But what about the females, because they also work together and live together and look after each other don't they? 

Drew - They do. I think that there's probably not as much interaction between females with the males. They spend a lot of time interacting with their children, and that probably disproportionately puts more emphasis on agreeableness for the males rather than the females.

Chris - And where do you think that openness influences the outcome for the females then; why does that make a difference to them but not the males?

Drew - Openness has to do with exploratory behavior. So these are individuals who tend to explore more thoroughly. There is a theory that this is the result of them living in captivity, because there's no downside to basically them exploring more. In the wild you would expect that individuals who explore too far would end up getting caught by a predator or contracting disease by poking around too much. And because there isn't any such dangers in captivity there's no downside to being more open.

Chris - The fact that you've got a range of different personality types, all within one big group of animals, does that mean then that - from an evolutionary point of view - nature is maintaining a range of personalities because they're are different outcomes for different individuals. If an individual is very aggressive, is very dominant but gets lots of mating in early but then gets killed nonetheless they've passed on a lot of genes; whereas an individual that is very agreeable, does get on very well with all the others, is well socially supported gets fewer mating opportunities but lives longer to invest more in their offspring. Is that what you think is emerging here?

Drew - That's definitely one of the possibilities. It's easy to understand how an individual who has many mating opportunities and has many children at a young age passes on their own genes. It's harder to understand how individuals who live longer are exactly profiting from that extra lifespan, but certainly rather more carefully investing in offspring over the course of a longer lifespan. It's definitely one way the individuals can improve their fitness...

Reconstruction of the 11.6-million-year-old fossil flying squirrel Miopetaurista neogrivensis.

24:52 - Fossil flying squirrel

How a rubbish tip surrendered the remains of the world's first complete skeleton of a flying squirrel...

Fossil flying squirrel
with Isaac Casanovas-Vilar, Universitat Autònoma de Barcelona

They say that where there’s trash there’s treasure; and in the case of the next story that’s certainly true, because the excavation of a new rubbish dump nearby gave Isaac Casanovas-Vilar the world’s first intact skeleton of a flying squirrel. As he explains to Chris Smith, he’s been able to use the specimen to settle a long-standing dispute between molecular biologists - who said these were recent evolutionary spin-offs, and palaeontologists, who claimed flying squirrels are much more ancient…

Isaac - This started with the building of a rubbish dump of a landfill 40 kilometres outside Barcelona in 2008 and many fossils have been recovered from these landfill, including primate specimens, and they found a block with a couple of femora; and it was taken to our preparation lab because they thought, initially, it was a primate. But when preparing they found that it was a rodent - a very large rodent!

Chris - So they were disappointed on one hand but then excited on the other because this was something very unusual?

Isaac - Yeah yeah yeah. But the beginning the only one that was excited was me, because it was - wow - it's a large size rodent with very slender limb bones. What can this be? And we had found some dental remains of flying squirrels. So we initially thought that this limb bones could fit with a large-sized flying squirrel. And when preparing the block we found a skull with those teeth as well. So then we were for sure that was the skeleton of a flying squirrel. This is the first time, and the only time we know, that there was a skeleton so we could have a complete picture of of the animal.

Chris - Why is this one so well preserved and so intact compared to every other specimen ever uncovered?

Isaac - Aha. That's because it was buried extremely fast. The animal died and it was not scavenged at all and it was covered by a mud flow that, with time, became mudstone. So the animal is intact with the bones - some of the bones even preserved in the original anatomical position - so the femurs are still attached to the pelvis the tail is still attached to the pelvis.

Chris - Now what did we know before you found this particular specimen? What did we know about the family tree, if you'll excuse the pun, of flying squirrels?

Isaac - Yeah, well, there was a major disagreement between palaeontologists and molecular biologists: molecular biologists studying the DNA of extant squirrel species found the flying squirrels originated from tree squirrels very recently - about 23 million years ago; whereas palaeontologists reported flying squirrels as old as thirty six million years ago. So that was a major disagreement - of more than 10 million years between - palaeontological and molecular data.

Chris - So how did this new specimen change things?

Isaac - Well, to tell if a squirrel actually glides or not you need the bones: you need the bones of the skeleton, particularly the wrist bones, which tells you if the animal had this flying membrane - that we call a patagium - to glide from tree to tree.

Chris - These bones of the little projections off the wrist aren't they - they're like an extra digit that helps to extend that membrane to create the gliding surface?

Isaac - Well it's actually a cartilage. So it's the same as your nose; the cartilage supporting the gliding membrane that is attached to a particular wrist bone. And then, when the flying squirrel jumps, it moves the hands - it rotates the hands inwards - and the flying membrane is extended so it can glide for many metres - sometimes more than 100 metres until the next tree.

Chris - So if you had that particular wrist appendage, you'd know what you were dealing with unequivocally?

Isaac - Yeah sure sure sure. So we put an additional effort to recover these small wrist bones. These are a few millimetres long. So when preparing the skeleton we insisted that all the sediment attached to the bones had to be screen-washed in order to recover the smallest fragment.

Chris - So what does that mean putting it through a sort of sieve so that you make sure you don't lose anything?

Isaac - Yeah yeah. That's it. All the sediment you remove, you put it through a sieve and then you wash it with the little bit of water. And, when sorting, we've found two of the wrist bones that turned out to be two of the three that support the cartilage of the potagium, so we were extremely happy that day, because it was "we did it", It was Eureka moment! We found them!

Chris - So that gives you the diagnosis. What about dating it. Can you date the block and work out therefore the context in which this animal is and therefore where in the timeline it sits?

Isaac - Yeah yeah. We have very accurate datings using techniques based on changes in magnetic polarity that gives you a precision of one hundred thousand years in the dating, so we know it is eleven point six million years ago. Knowing that, if we put it in a family tree with the extant flying squirrels then we can recalculate the dates of divergence of the different squirrel species and families and groups.

Chris - And when you do that how old does it turn out that this family tree is, because you were saying there's a bit of a controversy between one school of thought based on palaeontological findings and one school of thought based on genetic molecular findings and they disagree. So, actually, what is the correct answer based on what this fossil tells you?

Isaac - This isn't going to be the definitive answer, but for the moment we get older ages than the molecular biologists; we found that 23 million years ago is a possible age. But an age as old as 31 million years old for those splitting between the two lineages is as likely as that one...

ANCESTRAL-FLYING-SQUIRREL-SEMITRANSPARENT.jpg

Flying squirrel - Miopetaurista - semitransparent showing the skeleton overlaid with tissues

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