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Another bad day for anticipatory maternal effects

By Tobias Uller

A new study on water fleas, headed by Reinder and Alex, suggests that a classic example of adaptive maternal effects is not as adaptive as we might have thought.

Some years ago, Tobias, Sinead and Shinichi did a meta-analysis that seemed to undermine the idea that maternal effects are designed to transfer information about the local environment. Reviewers and editors did not really want to hear that, and the paper proved somewhat difficult to publish (but has been well received and cited). But one ‘anticipatory maternal effects’ appeared well supported: water fleas exposed to toxic cyanobacteria produced offspring that were more tolerant to the toxin.

So, to understand how this maternal effect evolves, Reinder and Alex challenged water flea mothers and offspring with cyanobacteria that produce the toxin microcystin. But rather than just expose the animals throughout their lives, they also exposed mothers at different times during her life. The rationale is that maternal effects that have been selected to transmit information are expected to behave like signals – triggered and delivered by a system well designed to pass on information with limited cost to the receiver.

It turned out that offspring indeed were somewhat better able to handle the toxin when their mothers had been exposed late in their lives. In other words, tolerance or resistance can be transmitted to the next generation through non-genetic means. But there was not much to suggest that the mechanism has been selected to transmit information about the presence of cyanobacteria. Instead, our experimental evidence – along with a meta-analysis of Daphnia research – fits better with a model of passive transfer of tolerance rather than an anticipatory maternal effect. Again, reviewers and editors were not very happy to hear this, and this paper also proved somewhat difficult to publish.

We should not be too surprised of these results, however. Not all plastic responses that allow organisms to cope with stress are properly seen as adaptations to cope with the stressor. We can think of these maternal effects as – in Mary-Jane West-Eberhard terms – examples of phenotypic accommodation that have not yet been followed by genetic accommodation.

But while our results question if there really has been selection for maternal transfer of information about microcystin exposure, the study is still not quite conclusive. Two kinds of follow-up studies would be particularly informative.

The first is to contrast responses of populations of water fleas with different evolutionary histories of exposure. This kind of comparison can effectively reveal if plastic responses in naïve animals become fine-tuned over evolutionary time (see a nice example from house finches here).

The second is to reveal the mechanism of the maternal effect. This would not only tell us ‘how it works’, but – keeping the comparison with signals in mind – whether or not the mechanism has properties that we expect of systems designed to transmit information.

We have our ideas about what is going on, and Alex has just completed a set of experiments that can tell us more. In the meantime, we hope that this paper will inspire more studies to look at maternal effects as a window into the evolutionary transition from stress-induced responses to local adaptation. To get started, please see here and here.

Tree Skinks Go To School: The Complexities of Social Learning in Lizards

By: Fonti Kar & Julia Riley

“Never study an animal that is smarter than you”

                   – Dr Martin Whiting

An adult female tree skink after performing the discrimination task we used to quantify their learning ability – she successfully removed the blue lid from this dish and accessed the food reward . Photo by Anna Küchler.

Animals learn about their environment and use what they have learnt while foraging, to increase mating success, avoid predators, and overall increase their chances of survival. An animal can learn by themselves, but this can be a long and difficult process. Alternatively, an animal can learn through the use of social information that is observed through “spying” on others. This is often an easier strategy, unless the social information is not accurate. We can relate to this – often when figuring out a problem, it’s easier to get help from a friend or teacher, rather than struggling through it on our own! In particular, social animals are likely to have more of a chance to observe others, and learn from them. We studied if tree skinks (Egernia striolata), a social Australian lizard, can learn from others.

Two tree skinks basking together beside a rock crevice in their natural habitat. Tree skinks are part of the Australian Egernia-group of social lizards, which across species, displays a diverse array of social and mating systems, including family-living and parental care. Photo by Martin Whiting.

In a previous study, we wanted to test whether adult female skinks can learn from another female. We trained a group of lizards to remove a lid to forage for some delicious fruit puree. In research, this type of challenge is called a ‘motor’ task. Once they were trained, this group of lizards demonstrated this action to another group of lizards that were naive to this foraging technique. Lizards in this ‘social learning’ group got to observe a demonstrating lizard before they attempted this motor task themselves. We compared this ‘social learning’ group to another group of lizards (our control) that needed to learn this task individually, without any help from others. We found that both ‘social learners’ and ‘individual learners’ (our control) were able to learn this motor task!

But, we then challenged the lizards with another, more complicated, task where they needed to learn to discriminate between dishes covered by a blue lid or a white lid. This was called the ‘discrimination task’. In this task the delicious food reward was accessible under the blue lid, but not the white lid. ‘Social learners’ made fewer errors and learnt this discrimination task a lot more quickly than ‘individual learners’ (our control). This means that that female tree skinks learn from one another! In complicated tasks, these social lizards likely use social information as a short-cut to learning.

Female tree skinks that were able to observe social information made fewer errors in the discrimination task, and learnt it more quickly than tree skinks that had to learn on their own. This shows that female tree skinks can socially learn! See the entire presentation Fonti Kar made on this study here.

Interestingly, we also investigated if juvenile tree skinks, that grew up in different social environments, used social information from an unfamiliar, adult female. We ran a similar experiment to our first, but also added a ‘reversal task’. In the reversal task, the food was now under the white lid. Lizards had to unlearn the rule from the previous, discrimination task (the food is under the blue lid), and now associate the white lid with a food reward (to see the methods for each of the tasks check out this video). In contrast to our previous study, we found no evidence that juveniles used social information from an unfamiliar, adult female. We were a bit surprised that juveniles did not use social information, because adult females do and it is often a beneficial short-cut to learning! But, the use of social information can vary depending on an animal’s age, and the environment and social context in which an animal develops or resides. In the wild, unfamiliar, unrelated, adult tree skinks can be lethally aggressive to juveniles in the wild. So, in our study, juveniles may not have been motivated to learn from an unknown adult that could, potentially, threaten their survival. A similar phenomenon has been observed in young guppies (Poecilia reticulata) – they don’t use social information from adults until they are large enough to not be impacted by aggressive advances of adults. All in all, we think that social feedback played a role in our finding that juvenile tree skinks did not use social information from unfamiliar, unrelated adult females.

Tree skink mothers often associate with their offspring, and this is thought to give them protection from other adult lizards that could, potentially, attack them. Photo by Julia Riley.

Learning is crucial for survival in the animal kingdom. Although we didn’t find evidence that juveniles would use social information presented by an unfamiliar, adult female, we did find that adult females socially learnt from one another. This is the first evidence that a family-living lizard is capable of learning from others!!! We also show that social learning is not guaranteed to be the default strategy of tree skinks. In fact, the use of social learning depends on a multitude of factors (i.e., the complexity of the task, the relationship between the demonstrator and learner, an individual’s age, etc.), and is likely only used when it benefits the learner.

Article references:

Whiting MJ, Xu F, Kar F, Riley JL, Bryne RW, and Noble DWA. 2018. Evidence for social learning in a family living lizard. Frontiers in Ecology and Evolution, doi: 10.3389/fevo.2018.00070

Riley JL,  Küchler A, Damasio T, Noble DWA, Byrne RW, Whiting MJ. 2018. Learning ability is unaffected by isolation rearing in a family-living lizard. Behavioural Ecology and Sociobiology, 72: 20, doi: 10.1007/s00265-017-2435-9

Brains and Brawn: Dominant lizards are better learners!

By Fonti Kar

Dominant individuals tend to have greater monopoly over food and mates and therefore have more offspring compared to subordinate individuals. Are these successes attributed to greater cognitive ability? Or are dominant individuals just better at freeloading from their clever subordinate counterparts?

We investigated whether dominant and subordinate eastern water skinks differ in their ability to learn from one and other (social learning). Previous work has shown in this species that young skinks tend to learn from older skinks, but age and dominance status and body size are inherently confounded. In other words, the age-dependent pattern may actually reflect a dominance effect, whereby young and therefore subordinate skinks tend to learn from older, dominant lizards.

In order to disassociate these confounding factors, we matched skinks closely in size and therefore age and allowed them to fight to determine their dominance statuses (Fig. 1). Winners of this fight was considered ‘dominant’, while the loser was considered ‘subordinate’. We then divided our skink pairs into two treatment groups, a ‘control’ group, where a skink watched their status counterparts do nothing and a ‘social learning’ group, where a skink was able to watch their status counterpart solve a foraging task e.g. a subordinate skink was able to watch a dominant skink, while a dominant skink was able to watch a subordinate skink (Fig. 2).

Control and social learning group set up. The control group watched their status counterparts do nothing. While the social learning group watched their status counterparts solve a task before receiving the task themselves

We gave the lizards two foraging tasks. In the first task, the lizards had to learn from their status counterparts how to learn to flip a blue lid to access a worm and ignore a white lid (association task). In the second task, the lizards had to unlearn the blue lid-worm association and learn to flip the white lid for the worm (reversal task). We then recorded how many trials it took for skinks to learn these tasks.

In the association task, skinks had to learn to flip the blue lid to access food. They then had to unlearn this association in the reversal task and learn to flip the white lid. See video below!

 

To our surprise, lizards did not seem to learn from the other lizard but instead relied on their own trial-and-error learning abilities. This was consistent for both dominant and subordinate lizards. We also found that dominant lizards learnt faster compared to subordinate lizards.

These results tell us a few neat things about social learning in the eastern water skink. Firstly, skinks were closely matched in size but they didn’t seem to learn from watching another skink. This seems to suggest that skinks may not want to learn from an individual of similar age and actually this may actually impede learning. Secondly, dominant individuals learnt faster compared to subordinate skinks implies that dominant skinks may be less prone to the stress associated with learning in the presence of another skink or they may indeed have both brains and brawn.

For more information, check out the paper published in Animal Cognition here