Department Aquatic Ecology

Eco-evolutionary interactions in space and time: the role of ECO-EVO-DEVO

Why this project?

The evolution of biological diversity is strongly facilitated by natural selection, both in space and time. Spatial environmental differences induce divergent natural selection, driving adaptive divergence and, ultimately, the evolution of reproductive isolation (i.e. ecological speciation). However, the propensity and degree of adaptive diversification may strongly depend on organismal dispersal and on geographic isolation (i.e. gene flow may counteract adaptive divergence and introduce novel genetic variation). Likewise, environments commonly fluctuate over time, giving rise to temporal shifts in selection.

Natural selection acts on the composite phenotype, which is the product of genetic variation and phenotypic plasticity. Hence, the determinants of phenotypic variation – and their mechanisms of inheritance (i.e. direct genetic and plastic effects, and transgenerational effects) – are of key importance for the evolution of biological diversity.

Our work here investigates the evolution of natural populations in response to interacting forces of selection and gene flow (in space and time), and the interactions between genetic variation, phenotypic plasticity (developmental plasticity) and transgenerational effects (in particular maternal investment in egg size) in diversification (an ECO-EVO-DEVO approach).

Study systems:

  • Threespine stickleback (Gasterosteus aculeatus) – in and around lake Myvatn, Iceland. Past work (by Räsänen) includes studies on lake-stream stickleback in the Misty lake, Canada.
  • Arctic charr (Salvelinus alpinus) – Dwarfed charr in complex of lava caves near Myvatn and resource polymorphic populations in multiple lakes across Iceland.

Approaches: Spatially and temporally replicated field surveys, population genetics, transcriptomics and laboratory rearing experiments.

Stickleback – Iceland:

  • Stickleback within lake Myvatn show phenotypic divergence in feeding morphology, body size, brain size and thermal performance across major habitat types within the lake. This divergence occurs in face of extensive gene flow (as reflected by microsatellite markers and lack of geographic barriers to dispersal).
  • At the same time, the stickleback population shows strong temporal fluctuations (across years) in population densities and phenotypic variation (e.g. age at maturation, body size and feeding morphology).
  • Recent rearing experiments indicate that this intra-lacustrine phenotypic divergence is due to a combination of direct genetic and plastic responses, as well as parental effects.
  • Stickleback across a pond complex (19 ponds) in the vicinity of lake Myvatn, show subtle phenotypic divergence and strong population genetic structure. Based on population genetic work, this divergence is likely strongly influenced by genetic drift in small populations, as well as different degrees of connectivity among ponds – mediated by seasonal flooding events.

Stickleback – Canada:

  • In the Misty lake system, the lake and inlet stream stickleback show extensive phenotypic and genetic divergence, whereas the lake and outlet stream stickleback show subtle divergence. Lake-stream divergence is facilitated by both genetic and plastic effects on phenotypes.
  • Intriguingly, there is an apparent lack of mating isolation between the lake and stream stickleback in the Misty system. This suggests that other mechanisms (e.g. temporal isolation or selection against migrants) maintain phenotypic and genetic divergence in this system.

Arctic charr – lava caves:

The cave charr present small (dwarfed) benthic phenotypes. The populations have small population sizes and show extensive population genetic structure across the caves and repeated parallel phenotypic divergence from the ancestral type of lake charr. Ongoing work on this system focuses on understanding evolutionary processes in small populations.

Arctic charr – lakes:

This work is ongoing, but first results (PhD thesis work of Samantha Beck) indicate that both egg size and variation in gene expression during juvenile development are key components of the evolution of resource polymorphism.

Publications

Conceptual

Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification

Adaptive diversification is driven by selection in ecologically different environments. In absence of geographical barriers to dispersal, this adaptive divergence (AD) may be constrained by gene flow (GF). And yet the reverse may also be true, with AD constraining GF (i.e. 'ecological speciation'). Both of these causal effects have frequently been inferred from the presence of negative correlations between AD and GF in nature - yet the bi-directional causality warrants caution in such inferences. We discuss how the ability of correlative studies to infer causation might be improved through the simultaneous measurement of multiple ecological and evolutionary variables. On the one hand, inferences about the causal role of GF can be made by examining correlations between AD and the potential for dispersal. On the other hand, inferences about the causal role of AD can be made by examining correlations between GF and environmental differences. Experimental manipulations of dispersal and environmental differences are a particularly promising approach for inferring causation. At present, the best studies find strong evidence that GF constrains AD and some studies also find the reverse. Improvements in empirical approaches promise to eventually allow general inferences about the relative strength of different causal interactions during adaptive diversification.
Räsänen, K.; Hendry, A. P. (2008) Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification, Ecology Letters, 11(6), 624-636, doi:10.1111/j.1461-0248.2008.01176.x, Institutional Repository

Maternal effects and evolution at ecological time-scales

1. Genetic and environmental maternal effects can play an important role in the evolutionary dynamics of a population: they may have a substantial impact on the rate and direction of genetic change in response to selection, and they may generate immediate phenotypic change via phenotypic plasticity. Because of this potential to generate rapid phenotypic change in a population, maternal effects may be particularly important for evolution at ecological time-scales.
2. Despite an increased interest in the prevalence, composition and adaptive benefits of maternal effects, little is still known of their impact on ecological and evolutionary processes in natural populations. We consider here the insights that a quantitative genetic framework provides into the pathways by which maternal effects can influence trait evolution in wild populations. Widespread evidence for a genetic basis of a range of maternal effects traits reinforces the notion that they cannot be treated as purely environmental sources of variation. We also provide an overview of the impact of environmental conditions on the expression and impact of maternal effects, and describe empirical evidence for their impact on evolution at ecological time-scales.
3. We emphasize the need for empirical work to quantify the associations between maternal and offspring phenotype and genotype, and the suite of selection pressures generated by maternal effects, as well as the relationship between maternal effects and environmental variation. Future work should aim to identify the conditions under which maternal effects are likely to play a role in evolution, as well as explicitly test the contribution of maternal effects to evolutionary responses.
Räsänen, K.; Kruuk, L. E. B. (2007) Maternal effects and evolution at ecological time-scales, Functional Ecology, 21(3), 408-421, doi:10.1111/j.1365-2435.2007.01246.x, Institutional Repository

Empirical

Does plasticity enhance or dampen phenotypic parallelism? A test with three lake–stream stickleback pairs

Parallel (and convergent) phenotypic variation is most often studied in the wild, where it is difficult to disentangle genetic vs. environmentally induced effects. As a result, the potential contributions of phenotypic plasticity to parallelism (and nonparallelism) are rarely evaluated in a formal sense. Phenotypic parallelism could be enhanced by plasticity that causes stronger parallelism across populations in the wild than would be expected from genetic differences alone. Phenotypic parallelism could be dampened if site-specific plasticity induced differences between otherwise genetically parallel populations. We used a common-garden study of three independent lake–stream stickleback population pairs to evaluate the extent to which adaptive divergence has a genetic or plastic basis, and to investigate the enhancing vs. dampening effects of plasticity on phenotypic parallelism. We found that lake–stream differences in most traits had a genetic basis, but that several traits also showed contributions from plasticity. Moreover, plasticity was much more prevalent in one watershed than in the other two. In most cases, plasticity enhanced phenotypic parallelism, whereas in a few cases, plasticity had a dampening effect. Genetic and plastic contributions to divergence seem to play a complimentary, likely adaptive, role in phenotypic parallelism of lake–stream stickleback. These findings highlight the value of formally comparing wild-caught and laboratory-reared individuals in the study of phenotypic parallelism.
Oke, K. B.; Bukhari, M.; Kaeuffer, R.; Rolshausen, G.; Räsänen, K.; Bolnick, D. I.; Peichel, C. L.; Hendry, A. P. (2016) Does plasticity enhance or dampen phenotypic parallelism? A test with three lake–stream stickleback pairs, Journal of Evolutionary Biology, 29(1), 126-143, doi:10.1111/jeb.12767, Institutional Repository

Spatial phenotypic and genetic structure of threespine stickleback (Gasterosteus aculeatus) in a heterogeneous natural system, Lake Mývatn, Iceland

Eco-evolutionary responses of natural populations to spatial environmental variation strongly depend on the relative strength of environmental differences/natural selection and dispersal/gene flow. In absence of geographic barriers, as often is the case in lake ecosystems, gene flow is expected to constrain adaptive divergence between environments – favoring phenotypic plasticity or high trait variability. However, if divergent natural selection is sufficiently strong, adaptive divergence can occur in face of gene flow. The extent of divergence is most often studied between two contrasting environments, whereas potential for multimodal divergence is little explored. We investigated phenotypic (body size, defensive structures, and feeding morphology) and genetic (microsatellites) structure in threespine stickleback (Gasterosteus aculeatus) across five habitat types and two basins (North and South) within the geologically young and highly heterogeneous Lake Mývatn, North East Iceland. We found that (1) North basin stickleback were, on average, larger and had relatively longer spines than South basin stickleback, whereas (2) feeding morphology (gill raker number and gill raker gap width) differed among three of five habitat types, and (3) there was only subtle genetic differentiation across the lake. Overall, our results indicate predator and prey mediated phenotypic divergence across multiple habitats in the lake, in face of gene flow.
Millet, A.; Kristjánsson, B. K.; Einarsson, Á.; Räsänen, K. (2013) Spatial phenotypic and genetic structure of threespine stickleback (Gasterosteus aculeatus) in a heterogeneous natural system, Lake Mývatn, Iceland, Ecology and Evolution, 3(10), 3219-3232, doi:10.1002/ece3.712, Institutional Repository

Connectivity in a pond system influences migration and genetic structure in threespine stickleback

Neutral genetic structure of natural populations is primarily influenced by migration (the movement of individuals and, subsequently, their genes) and drift (the statistical chance of losing genetic diversity over time). Migration between populations is influenced by several factors, including individual behavior, physical barriers, and environmental heterogeneity among populations. However, drift is expected to be stronger in populations with low immigration rate and small effective population size. With the technological advancement in geological information systems and spatial analysis tools, landscape genetics now allows the development of realistic migration models and increased insight to important processes influencing diversity of natural populations. In this study, we investigated the relationship between landscape connectivity and genetic distance of threespine stickleback (Gasterosteus aculeatus) inhabiting a pond complex in Belgjarskógur, Northeast Iceland. We used two landscape genetic approaches (i.e., least-cost-path and isolation-by-resistance) and asked whether gene flow, as measured by genetic distance, was more strongly associated with Euclidean distance (isolation-by-distance) or with landscape connectivity provided by areas prone to flooding (as indicated by Carex sp. cover)? We found substantial genetic structure across the study area, with pairwise genetic distances among populations (DPS) ranging from 0.118 to 0.488. Genetic distances among populations were more strongly correlated with least-cost-path and isolation-by-resistance than with Euclidean distance, whereas the relative contribution of isolation-by-resistance and Euclidian distance could not be disentangled. These results indicate that migration among stickleback populations occurs via periodically flooded areas. Overall, this study highlights the importance of transient landscape elements influencing migration and genetic structure of populations at small spatial scales.
Seymour, M.; Räsänen, K.; Holderegger, R.; Kristjánsson, B. K. (2013) Connectivity in a pond system influences migration and genetic structure in threespine stickleback, Ecology and Evolution, 3(3), 492-502, doi:10.1002/ece3.476, Institutional Repository

Genetic and plastic contributions to trait divergence between parapatric habitats: female life-history traits in threespine stickleback within the Misty Lake system

Question: How do genetic and plastic effects on maternal investment influence divergence between parapatric populations that do or do not show high gene flow? How might these patterns influence adaptation and progress towards ecological speciation?
Organisms: Wild-caught and laboratory-reared lake, inlet stream, and outlet stream threespine stickleback (Gasterosteus aculeatus) from the Misty Lake system, northern Vancouver Island, British Columbia, Canada. In nature, the inlet–lake pair shows low gene flow, whereas the outlet–lake pair shows high gene flow.
Methods: Analysis of covariance was used to compare egg size (dry mass), clutch size (number of eggs = fecundity), and clutch mass (dry mass = reproductive effort) among habitats (lake, inlet, outlet) and between rearing environments (wild, laboratory). Body size was used as a covariate to consider life-history variation relative to body size.
Results: In the wild, inlet females had greater reproductive effort and higher fecundity than did lake females, both before and after correction for body size. Outlet females were intermediate but closer to lake females, and showed clines in life-history traits with distance from the lake. In the laboratory, differences in these traits were in a similar direction but smaller. Differences between habitats in reproductive effort and clutch size are thus shaped by complementary (co-gradient) contributions from genetic differences and plasticity. Egg size did not vary between the habitats and was not plastic.
Conclusions: Outlet females were estimated to have a 32–71% decline in reproductive output in the wild – but this maladaptation would have been greater in the absence of plasticity. These modifying effects of plasticity on maladaptation will influence gene flow and progress towards ecological speciation.
Baker, J. A.; Räsänen, K.; Moore, J.-S.; Hendry, A. P. (2013) Genetic and plastic contributions to trait divergence between parapatric habitats: female life-history traits in threespine stickleback within the Misty Lake system, Evolutionary Ecology Research, 15(4), 473-487, Institutional Repository

Extreme sexual brain size dimorphism in sticklebacks: a consequence of the cognitive challenges of sex and parenting?

Selection pressures that act differently on males and females produce numerous differences between the sexes in morphology and behaviour. However, apart from the controversial report that males have slightly heavier brains than females in humans, evidence for substantial sexual dimorphism in brain size is scarce. This apparent sexual uniformity is surprising given that sexually distinct selection pressures are ubiquitous and that brains are one of the most plastic vertebrate organs. Here we demonstrate the highest level of sexual brain size dimorphism ever reported in any vertebrate: male three-spined stickleback of two morphs in an Icelandic lake have 23% heavier brains than females. We suggest that this dramatic sexual size dimorphism is generated by the many cognitively demanding challenges that males are faced in this species, such as an elaborate courtship display, the construction of an ornate nest and a male-only parental care system. However, we consider also alternative explanations for smaller brains in females, such as life-history trade-offs. Our demonstration of unprecedented levels of sexual dimorphism in brain size in the three-spined stickleback implies that behavioural and life-history differences among the sexes can have strong effects also on neural development and proposes new fields of research for understanding brain evolution.
Kotrschal, A.; Räsänen, K.; Kristjánsson, B. K.; Senn, M.; Kolm, N. (2012) Extreme sexual brain size dimorphism in sticklebacks: a consequence of the cognitive challenges of sex and parenting?, PLoS One, 7(1), e30055 (4 pp.), doi:10.1371/journal.pone.0030055, Institutional Repository

Divergent selection and then what not: the conundrum of missing reproductive isolation in Misty Lake and stream stickleback

In ecological speciation, reproductive isolation evolves as a consequence of adaptation to different selective environments. A frequent contributor to this process is the evolution of positive assortative mate choice between ecotypes. We tested this expectation for lake and inlet stream threespine stickleback (Gasterosteus aculeatus) from the Misty system (Vancouver Island, Canada), which show strong genetically based adaptive divergence and little genetic exchange in nature. This, and work on other stickleback systems, led us to expect positive assortative mating. Yet, our standard “no-choice” laboratory experiment on common-garden fish revealed no evidence for this—despite divergence in traits typically mediating assortative mating in stickleback. These results remind us that divergent natural selection may not inevitably lead to the evolution of positive assortative mate choice. The apparent lack of strong and symmetric reproductive barriers in this system presents a conundrum: why are such barriers not evident despite strong adaptive divergence and low gene flow in nature?
Räsänen, K.; Delcourt, M.; Chapman, L. J.; Hendry, A. P. (2012) Divergent selection and then what not: the conundrum of missing reproductive isolation in Misty Lake and stream stickleback, International Journal of Ecology, 2012, 1-14, doi:10.1155/2012/902438, Institutional Repository

Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation

Ecological selection against hybrids between populations occupying different habitats might be an important component of reproductive isolation during the initial stages of speciation. The strength and directionality of this barrier to gene flow depends on the genetic architecture underlying divergence in ecologically relevant phenotypes. We here present line cross analyses of inheritance for two key foraging-related morphological traits involved in adaptive divergence between stickleback ecotypes residing parapatrically in lake and stream habitats within the Misty Lake watershed (Vancouver Island, Canada). One main finding is the striking genetic dominance of the lake phenotype for body depth. Selection associated with this phenotype against first- and later-generation hybrids should therefore be asymmetric, hindering introgression from the lake to the stream population but not vice versa. Another main finding is that divergence in gill raker number is inherited additively and should therefore contribute symmetrically to reproductive isolation. Our study suggests that traits involved in adaptation might contribute to reproductive isolation qualitatively differently, depending on their mode of inheritance.
Berner, D.; Kaeuffer, R.; Grandchamp, A. C.; Raeymaekers, J. A. M.; Räsänen, K.; Hendry, A. P. (2011) Quantitative genetic inheritance of morphological divergence in a lake-stream stickleback ecotype pair: implications for reproductive isolation, Journal of Evolutionary Biology, 24(9), 1975-1983, doi:10.1111/j.1420-9101.2011.02330.x, Institutional Repository

Genetic divergence in morphology–performance mapping between Misty Lake and inlet stickleback

Different environments should select for different aspects of organismal performance, which should lead to correlated divergence in morphological traits that influence performance. The result should be genetic divergence in aspects of performance, morphology and associations (‘maps’) between morphology and performance. Testing this hypothesis requires quantifying performance and morphology in multiple populations after controlling for environmental differences, but this is rarely attempted. We used a common-garden experiment to examine morphology and several aspects of swimming performance within and between the lake and inlet populations of threespine stickleback (Gasterosteus aculeatus) from the Misty system, Vancouver Island, Canada. Controlling for body size, lake stickleback had shallower bodies, larger caudal fins and smaller pelvic girdles. With or without morphological covariates, lake stickleback showed greater performance in both sustained and burst swimming. In contrast, inlet stickleback showed greater manoeuverability than did lake stickleback in some analyses. Morphology–performance relationships were decoupled when considering variation within vs. between populations. Moreover, morphology–performance mapping differed between the two populations. Based on these observations, we advance a hypothesis for why populations adapting to different environments should show adaptive genetic divergence in morphology–performance mapping.
Hendry, A. P.; Hudson, K.; Walker, J. H.; Räsänen, K.; Chapman, L. J. (2011) Genetic divergence in morphology–performance mapping between Misty Lake and inlet stickleback, Journal of Evolutionary Biology, 24(1), 23-35, doi:10.1111/j.1420-9101.2010.02155.x, Institutional Repository

Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback

Mating isolation is a frequent contributor to ecological speciation – but how consistently does it evolve as a result of divergent selection? We tested for genetically based mating isolation between lake and stream threespine stickleback (Gasterosteus aculeatus L.) from the Misty watershed, Vancouver Island, British Columbia. We combined several design elements that are uncommon in the studies of stickleback mate choice: (i) we used second-generation laboratory-reared fish (to reduce environmental and maternal effects), (ii) we allowed for male–male competitive interactions (instead of the typical no-choice trials) and (iii) we included hybrids along with pure types. Males of different types (Lake, Inlet, hybrid) were paired in aquaria, allowed to build nests and then exposed sequentially to females of all three types. We found that Lake and Inlet males differed in behaviours thought to influence stickleback mate choice (inter- and intra-sexual aggression, display and nest activities), whereas hybrids were either intermediate or apparently ‘inferior’ in these behaviours. Despite these differences, Lake and Inlet fish did not mate assortatively and hybrid males did not have a mating disadvantage. Our study reinforces the noninevitability of mating isolation evolving in response to ecological differences and highlights the need to further investigate the factors promoting and constraining progress towards ecological speciation.
Raeymaekers, J. A. M.; Boisjoly, M.; Delaire, L.; Berner, D.; Räsänen, K.; Hendry, A. P. (2010) Testing for mating isolation between ecotypes: laboratory experiments with lake, stream and hybrid stickleback, Journal of Evolutionary Biology, 23(12), 2694-2708, doi:10.1111/j.1420-9101.2010.02133.x, Institutional Repository

Related student projects

Ph.D. theses

Antoine Millet (2013) Spatio-temporal environmental and morphological variation in a dynamic natural system, Lake Myvatn threespine stickleback. (Univ. of Iceland/Holar Univ. College, Iceland).

M.Sc. theses

Coralie Delrue (ongoing) Diet and temperature mediated phenotypic divergence in threespine stickleback from lake Myvatn, Iceland: phenotypic plasticity vs. genetic divergence. Holar Univ. College, Iceland

Tamara Diethelm. (2011) Maternal investment and maternal effects in threespine stickleback (Gasterosteus aculeatus) inhabiting contrasting temperatures”. Dept. of Biology, ETH-Zurich, Switzerland.

Matthew Seymour. (2011) Threespine sticklebacks (Gasterosteus aculeatus) in Belgjarskógur, Iceland: Phenotypic and genetic divergence at a small spatial scale. Holar Univ. College, Iceland.

Mike Senn (2010) Divergence in reproductive traits of threespine stickleback inhabiting contrasting temperatures. Univ. of Zurich, Switzerland.

Andrea Koopmans (2010) Divergence in functional morphology: diet and gill raker structure in threespine stickleback (Gasterosteus aculeatus) in Lake Mývatn, Iceland. Dept. of Environmental sciences, ETH-Zurich, Switzerland.

Vera Gräzer (2009) Adaptive Divergence in Reproductive Traits and Behaviour: Do Nest Site Choice, Maternal Investment & Parental Care Differ among three Ecotypes of Icelandic Threespine Stickleback, Gasterosteus aculeatus? Dept. of Biology, ETH-Zurich, Switzerland.

Matthieu Delcourt (2006) Reproductive isolation in threespine stickleback (Gasterosteus aculeatus). McGill University, Canada. 

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