Eco-evolutionary dynamics of partial migrations

I am currently working as a postdoctoral researcher with Prof. Jane Reid at the Norwegian University of Science and Technology. I am fortunate to take part in the ongoing long-term study on European shags Phalacrocorax aristotelis in Scotland, in collaboration with the University of Aberdeen and the UK Centre for Ecology and Hydrology. This fascinating system is a partially migratory metapopulation (PMMP). Partial migration is when some individuals remain in the breeding colony all year round, whereas the other half migrate elsewhere overwinter. In the case of the shags, many of the migrant destinations are other breeding colonies, where the resident birds also do their own thing of staying or going. This creates a metapopulation of separate breeding colonies interlinked by seasonal migrants, and the eco-evolutionary dynamics of such systems are the topic of my postdoc! Important and unanswered questions include:

• What can (and can't) traditional theory on partial migration tell us about the evolution of such PMMPs? How do PMMPs arise?

• How do PMMPs respond to changes in environmental conditions, with regards to evolutionary and population dynamics?

• Might extreme climatic events in certain locations lead to ecological and/or evolutionary ripple effects throughout the PMMP?

Watch this space for more updates, and please get in touch if you have questions/input! First preprint is now out!

The evolution of sex

I worked for 2 1/2 years as a postdoctoral researcher in Hanna Kokko's lab at the University of Zürich. As a professional Kokkonut, I worked on topics related to the evolution of sexual reproduction, including the dynamics of facultative sex versus obligate sexuality or asexuality, in organisms with different life-histories, ecological conditions and evolutionary constraints.

In one project, now termed the "grand sex project", we aim to investigate the effects of different kinds of assumptions modellers make about the types of organisms they model when researching the evolution of sex. Facultatively sexual organisms span from mostly sexual vertebrates, where females only resort to parthenogenesis as a "last resort"; via hermaphrodites in the animal and plant kingdoms who can reproduce both by outcrossing, selfing, or asexually; to fungi and microorganisms who may not even have sexes (anisogamy) but rather two or more isogamous mating types. Who can mate with whom? What happens if you fail to find a suitable mate? With help from Isobel Booksmythe (now in Australia), we have reviewed the theoretical literature on the evolution of sex and classified all 250+ models according to these and other questions about what kind of life cycle the authors are (explicitly or implicitly) assuming that their modelled organisms exhibit. I now aim to use simulation models spanning these different life cycles in order to illustrate the pitfalls of using too narrow a scope - and to see whether we can find out why people still disagree on whether or not the "paradox of sex" has been resolved.

Facultative sex and sex-limited gene expression

In another project, motivated by lockdown zoom chats with Prof. Dieter Ebert (University of Basel), I use a population genetics model to investigate the strength of selection on male- or female-limited loci in facultatively sexual species. The original thought was: If for example males occur very rarely in these species (such as Daphnia, or C. elegans), then genes responsible for their function should be under much weaker selection and may suffer from mutational degradation. This is true (and has been shown) for other cases of conditional gene expression (see e.g. Van Dyken & Wade 2010 Genetics), such as genes only expressed under certain rare environmental conditions, but it stops being true for male- or female-limited expression if the females can reproduce both sexually and asexually. What matters for selection on male-specific loci isn't how many males there are or how often, but rather how many offspring have a father - which depends on the extent to which females decide to reproduce sexually versus asexually. This work is now on biorXiv as a preprint. Questions and feedback welcome!

With: Hanna Kokko, Isobel Booksmythe (Monash University), Dieter Ebert (University of Basel).

Acknowledgements: Denis Roze for input on the grand sex project; all the current and former Kokkonuts for making these 2 1/2 so worthwhile!

I am very interested in new collaborations - feel free to contact me if you have any ideas or just want to chat!

Ph. D. research: Adaptations to variable and unpredictable environments

Anthropogenic climate change is causing rapid changes in living conditions for organisms around the globe. Importantly, the environments organisms experience are changing not only in their mean conditions (e.g. becoming warmer, wetter, drier...), but also in how variable or predictable conditions are. There has been a lot of work done on how organisms should deal with such variation on different time scales. While the field of behavioral ecology has typically focused on short-term variation and within-generation adaptations (e.g. insurance, risk-sensitivity), this has seldom taken a long-term view and considered that conditions may change between generations as well, affecting the optimal behaviors in an individual's lifetime. Such problems have rather been dealt with by evolutionary biologists, who have identified key concepts such as bet-hedging strategies and phenotypic canalization. However, these various adaptations to short- and long-term environmental variability have rarely been placed in the same framework, and it is not always clear how they relate to each other, whether and how they will interact, and to what extent they are even mutually compatible.

The approach of my Ph.D. project was therefore to use a variety of theoretical modelling tools to link short- and long-term adaptations to uncertainty and unpredictability. We took well-established concepts within behavioral ecology, and applied an evolutionary perspective where the environment varies both within and between generations. Below is a summary of these papers and some ongoing work in the same vein.

Insurance, bet-hedging and canalization: Phenotypic evolution in a variable environment

In the first paper of my Ph.D., I use skewed fitness functions to investigate the effects of insurance and conservative bet-hedging in coping with within- and between-generation environmental variability. I show that the relative importance of conservative bet-hedging depends on the amount of diversifying bet-hedging (adaptive phenotypic variation among offspring), and confirm and expand on previous results from the theoretical literature. This work is published in Evolution (Haaland, T.R., Wright, J., Tufto, J., Ratikainen, I.I. 2019), and I wrote a popular science piece about it for the science outreach blog Ecology for the Masses.

With: Irja Ida Ratikainen, Jarle Tufto, Jonathan Wright (all NTNU).

Acknowledgements: Luis-Miguel Chevin and Andrew Simons for valuable discussions.

Specialist, generalists and bet-hedgers: Phenotypic variability within and between individuals

Using the same framework as in the above paper, I investigate how within-individual phenotypic variability (which can be seen as for example niche width) affects the adaptive advantage of between-individual variability, such as diversifying bet-hedging. This work is still in preparation, but promises to reveal exciting insights. I identify different strategies depending on whether the traits we are interested in cause fitness to accumulate additively (for example in foraging related traits) or multiplicatively (for traits directly affecting survival probability), and depending on how the environmental conditions vary within and between generations. In what cases might generalism represent a bet-hedging strategy? When is it better to produce very different (bet-hedged) specialist offspring, than very similar generalist offspring

This paper is now pubished in Oikos - check it out here!

With: Irja Ida Ratikainen and Jonathan Wright

Acknowledgements: Lovely, underappreciated papers by Michael Lynch, Wilfred Gabriel and George Gilchrist.

Adaptation to rare events: What can evolutionary history tell us about vulnerability to climate change?

Instigated during a research stay at Dr. Carlos Botero's lab at Washington University in St. Louis, USA, I have built a series of models on the relative importance of additive and multiplicative fitness accumulation in evolutionary processes. Additive fitness accumulation occurs in traits that are subject to many selective events in each individual's lifetime, and in heterogeneous environments where individuals in a populations experience different conditions in the same generation. Conversely, multiplicative fitness accumulation occurs in traits that are subject to one or few selective events in each lifetime, and in homogeneous environments where all or most individuals in a population experiences the same conditions each generation. These different modes of fitness accumulation can select for very different traits in the long term, and we are interested in how these different traits can leave populations differentially vulnerable to ongoing global changes in extreme weather events such as floods, droughts, wildfires and hurricanes. I'm thrilled that this work is now published in Ecology and Evolution (Haaland, T.R. & Botero, C.A. 2019), and has received media coverage!

During my stay in Dr. Botero's lab I also helped develop experimental procedures to test these predictions empirically, on the yeast Saccharomyces cervisiae. These experiments are currently under way. Combined with results from our models where climate change leads to different types of changes in the regimes of extreme events, we hope that this work can reveal new insights for setting conservation priorities in the face of anthropogenic climate change.

With: Carlos Botero. 

Acknowledgements: Vince Fasanello, Suchith DaSilva, Justin Fay and Ping Liu for work and help with the yeast lab; Jeremy Van Cleve, Joanna Masel and Samuel Scheiner for theoretical input.

Phenotypic plasticity as a bet-hedging strategy

Springing out at the tail end of my Ph.D. was one more topic that began to interest me more and more: The possibility of phenotypic plasticity at the individual level acting as a bet-hedging strategy at the genotype level. Although plasticity and bet-hedging are both well-studied modes of response to environmental variability and climate change, they are usually only considered as alternatives to each other. However, during my Ph.D. work linking adaptations on different evolutionary time scales, I realized that bet-hedging might in fact be acting on plastic responses themselves. Therefore, combining the approaches taken in my previous Ph.D. papers I modelled the evolution of reversible plasticity in organisms with different life-histories and environmental backgrounds. I also applied our results to empirical data of responses in breeding phenology to variation in spring temperature, with important insights for tracking how organisms respond to anthropogenic climate change. Specifically, while it is well-known that species with shorter generation times are likely to better track a warming climate through microevolutionary changes (due to faster response to selection), we show that these species are also more likely to exhibit bet-hedging adaptations in terms of stronger plastic responses. Long-term individual-level studies are needed in order to tease apart the relative roles of plasticity and adaptive tracking.

This work is now out in Journal of Evolutionary Biology - have a look!

With: Jonathan Wright, Maja Tarka (Lunds Universitet), Irja Ratikainen.

Acknowledgments: The lovely meta-analysis by Radchuk et al. (2019 Nat. Comms.) of animal responses to climate change upon which we based our empirical analysis

Other projects

Seed size variability in Dalechampia: Are perennial plants hedging their bets?

Seed dormancy is important for coping with unpredictable rainfall patterns, and variation in duration of dormancy in desert annuals has become a quintessential example of bet-hedging in natural systems. Fueled by the observation of variation in seed size in the neotropical vine Dalechampia scandens, I set out together with former Kokkonut Hanna ten Brink (now at EAWAG) and former CBD member Øystein Opedal (now at Lunds Universitet) on a project investigating the evolution of seed dormancy in response to within- and among-year variation. Dalechampia live in environments spanning from highly seasonal (with a defined dry and wet season) to less seasonal, and the consequences of too much (or too little) dormancy should thus vary across populations and ecotypes. Not much work has been done on bet-hedging and seed dormancy in perennial plants before, and we therefore look forward to producing predictions for optimal seed dormancy under different levels of among- and within-year rainfall variability, which can be verified with empirical data on Dalechampia.

This work is now published in Evolution!

With: Hanna ten Brink, Øystein Opedal, Francois Massol

Acknowledgements: Hanna Kokko (University of Mainz); Dalechampions in Christophe Pélabon's lab at NTNU.

How do you track a changing environment over time, and when should you not bother? 

I have worked on simulation models exploring the evolution of learning and sampling in a variable and unpredictable environment. Climate change is causing problems for organisms that rely on environmental cues such as photoperiod or temperature. Cues that previously were reliable indicators of when to start breeding are now causing phenological mismatch for species in many parts of the world. Animals can also base their decision on own experience - what worked well last year? If conditions are likely to be similar to the last time the decision was made (temporal autocorrelation), relying on memory may be a good strategy.

Here I allow genes for plasticity, sampling effort and memory to co-evolve under different degrees of temporal autocorrelation and cue reliability. I am then interested in exploring how well the evolved strategies perform when one of these environmental parameters change - which is what humans are doing to animals now. By making weather more extreme and unpredictable, by warming the planet and shifting the onset of spring, by removing or decoupling links between cues used by organisms and fitness-relevant information, we are posing novel challenges to animals around the world, and it is therefore important to know how or whether they will be able to keep up with these new conditions in the future.

This work is now published in a grand Biological Reviews paper on learning in a behavioural reaction norm context.

With: Jonathan Wright, Irja Ida Ratikainen, Niels Dingemanse (LMU Munich), Dave Westneat (University of Kentucky).

Acknowledgements: Carlos Botero (WUSTL), Trevor Fristoe (University of Konstanz) and Aimee Dunlap (UMSL) for helpful discussions.

Sexual selection and parental care 

For my Master's degree at NTNU I created a state-based stochastic dynamic model of the differential allocation hypothesis - that parents adjust their investment in offspring depending on the quality or attractiveness of their current mate. I have continued working on this topic on the side of my Ph. D. work, as it is an intriguing problem attracting a lot of attention from behavioural ecologists and evolutionary biologists alike.

This work has resulted in two publications, one presenting my stochastic dynamic model alongside an analytical model which supports our results (Haaland, T.R., Wright, J., Kuijper, B., Ratikainen, I. I.; 2017 Am. Nat., open access!), and one where we extend the stochastic dynamic model to investigate how mate quality can affect the trade-off between offspring size and number (Ratikainen, I. I., Haaland, T. R., Wright, J.; 2018 Proc R. Soc. B., also open access).

I have co-supervised an MSc project testing the logic behind Burley's original formulation of the differential allocation hypothesis: That investing more when you're with a high-quality mate is beneficial because it increases the chance of this mate staying with you until the next breeding season. While this argument has all but been abandoned in discussions of differential allocation since, we tested whether the predictions from our Haaland et al 2017 model still hold when allowing for this effect. In order to critically test the conclusions from this model, we are currently looking into an adaptive dynamics model of the evolutionary feedbacks between mate choice and differential allocation at the population level, in collaboration with Eva Kisdi and Tadeas Priklopil.

Acknowledgements: Hanna Kokko, Andy Higginson, Franjo Weissing.

Arctic fox behaviour and conservation

In collaboration with the researchers from Stockholm University in Sweden, I have been gathering field data on the critically endangered Scandinavian Arctic foxes (Vulpes lagopus) and assisted with conservation measures such as tagging, monitoring and sampling foxes and cubs for population inventory, vaccination, supplementary feeding, assessing habitat quality (vegetation analysis) and food availability (bird inventory, rodent trapping to monitor long-term cycles). Observing the foxes day and night for months during the Arctic summer, I am now interested in developing models to examine the reproductive decisions, territorial behavior, division of labour, dispersal and predation risk of Arctic fox families. Hunted to near extinction about 100 years ago, Arctic foxes have failed to recover after their protection, as they are faced with a number of threats, such as inbreeding depression due to low population sizes, low connectivity between subpopulations, diseases and competition from red foxes and lower food availability due to climate change. Arctic fox families are facing different challenges than before, and understanding their behavioural dynamics can therefore help us predict how they will react to future conditions, and allow us to make more effective conservation measures.

With: Sinah Haussmann, Hanna Kokko (both University of Zürich); Anders Angerbjörn, Rasmus Erlandsson (both University of Stockholm).

Using IT tools for teaching in field courses

I have been teaching botany labs and field trips on the undergraduate course Floristics and Faunistics in Norwegian Ecosystems in 2015-2017, and have designed an experiment to test the short- and long-term learning outcome of using Geographic Information Systems (GIS) in the field.

With: Kristiane Midtaune, Jakob Bonnevie Cyvin, Jan Ketil Rød, Department of Geography, NTNU; Sigrid Lindmo, Ragnhild Thorsen Grevskott, Department of Biology, NTNU.

Game theory, behavioral reaction norms and information use in a variable world

Game theory concerns itself with situations where two or more individuals (players) interact, and where the best decision for each player depends on the actions of the other player(s). While much has been said and done about this rich and fascinating field - also within the realms of animal behaviour - a predictive theory about how variable environments affect individual decisions has been lacking. I am interested in exploring the evolution of social behavioural reaction norms, that is, how an individual should behave depending on its social environment.

So far I have been focusing on a social foraging case known as the Producer-Scrounger game, but the concepts are easily extended to other game theoretical problems. I go beyond traditional ESS theory in which stable frequencies of strategies within a population are well established, to investigate the strategies (reaction norms) of the individuals that make up the population. When the population is at the ESS, all individuals by definition do equally well. But how does the population arrive here? Do certain individuals always use one or the other strategy, regardless of what the others are doing? Or are they plastic, i.e. always responding to their social environment? If so, how do they gather this? Is private information better than public information in deciding which tactic to use? These are only some of the questions that can be addressed with this novel approach to a well-known field of research.

With: Jonathan Wright, Irja Ida Ratikainen, Dhanya Bharath, Micah Brady

Acknowledgements: Håkon Johansen for getting the project a flying start with his modeling and writing; Arnon Lotem, Aimee Dunlap and Carlos Botero for valuable discussions.