Individuals differ: does it matter? A special issue on individual heterogeneity in Oikos (May 2018)

Individuals, be they plants or animals, are rarely equal. Does it matter that individuals differ? More specifically, what are the consequences for the dynamics of populations of such differences between individuals, also referred to as individual heterogeneity? And how does individual heterogeneity affect the evolution of traits? The scientific journal Oikos has just published a special issue with a collection of papers that tackle such questions.

In one of the papers of this special issue, I, together with two master students Jasper Croll and Rianne Fernandes, investigated how the structure and size of populations of bulb mites (Rhizoglyphus robini) changed after selectively harvesting either adult fighter males or adult scrambler males from single populations [1]. These two types of adult bulb mite males are very different: fighters have thickened legs with sharp ends that they can use to kill other mites (on the left in photo below), whereas scramblers do not have such modified legs (on the right in photo below). The two types of males nearly always occur together in single populations.

cropped-mite-photo-for-blog.jpg

We expected that if we removed fighters (or scrastudy organismsmblers) from a population, this would, over a number of generations, result in an evolutionary shift in male morph expression resulting in a reduction in the frequency of fighters (or scramblers). We tested this hypothesis in the lab where we have populations of bulb mites in small glass tubes (photo on the right). Using a microscope, we can count the number of mites in these populations, and also measure their size, sex and male morph. However, we found a completely different response to our experimental treatments. In the populations where we selectively harvested fighters, we found that this resulted in even more fighters in the populations!

So what was happening? We conducted another experiment where we investigated the killing behaviour of single fighter males that were put together with a single juvenile mite (remember: fighters can kill other mites with their dagger-like legs). Of the juveniles that survived to adulthood in the presence of a fighter, we found that hardly any of them matured into fighters. In our control treatment where single juveniles were kept without an adult fighter, we did find that most males matured as fighters. These results suggest that adult fighters are able to assess which juvenile males are most likely to turn into a fighter, and killed them before they were able to develop their weaponry (only adult fighters have the dagger-like legs). If this indeed was the case, then, in our previous experiment, by removing adult fighters, more juvenile males matured as a fighter. Thus, by selectively removing adult fighters, we increased the likelihood that juvenile males survived till adulthood to become a fighter, which would explain why we observed a higher number of fighters in experimental treatment where we removed adult fighters.

Although what we observed sounds counterintuitive, this phenomenon has been observed quite often in nature and it is called an overcompensatory response [2]. The most important conclusion from this work is that differences between individuals (individual heterogeneity) affects the response to selection (in our case by selective harvesting) and, at the same time, the size and structure populations. All this complicates our ability to accurately predict how populations respond to changes, for example those imposed by changes in the environment (climate change). One of the conclusions of the Oikos special issue is also that “We still have far to go before we reach a deep understanding of the causes and consequences of individual heterogeneity” [3].

So, you might think, why does all this matter? For one, we need a thorough understanding of the mechanisms that underlie the responses of populations to environmental change in order to understand drivers of biodiversity and prevent its (further) loss. In this respect, the United Nations has set a Sustainable Development Goal (SDG 15) for 2030 [4] to achieve precisely this. The International Union for Conservation of Nature (IUCN) is crucial in catalysing actions for biodiversity conservation and policy change. Such actions are informed by demographic quantities of threatened populations [e.g. 5], like the rate of population growth or generation time, but which are often calculated without including mechanisms of development, genetics and demography; all of which fuel individual heterogeneity. Indeed, I have shown that including these more realistic aspects can result in diametrically opposed conservation inferences [6]. So, as also advocated in the Oikos special issue, understanding the factors involved in how populations respond to environmental change will help us predict these responses in the context of future environmental change. In this way, work like this should be able to contribute to creating meaningful strategies for mitigation of unwanted environmental change effects on populations and biological diversity.

References

1 Smallegange IM, Fernandes RE, Croll JC. 2018. Population consequences of individual heterogeneity in life histories: overcompensation in response to harvesting of alternative reproductive tactics. Oikos 127: 738-749.

2 Schröder, A. et al. 2014. When less is more: positive population-level effects of mortality. Trends in Ecology and Evolution 29: 614–624.

3 Hamel S, Yoccoz NG, Gaillard J-M, Bassar RD, Bouwhuis S, Caswell H, Douhard M, Gangloff EJ, Gimenez O, Lee PC, Smallegange IM, Steiner UK, Vedder O, Vindenes Y. 2018. General conclusion to the special issue Moving forward on individual heterogeneity. Oikos. 127: 750-756.

4 United Nations General Assembly: Transforming Our World: The 2030 Agenda for Sustainable Development. Draft resolution referred to the United Nations summit for the adoption of the post-2015 development agenda by the General Assembly at its sixty-ninth session. UN Doc. A/70/L.1 of 18 September 2015.

5 Smallegange IM, van der Ouderaa IBC, Tibiriça Y. (2016) The effect of yearling, juvenile and adult survival on reef manta ray (Manta alfredi) demography. PeerJ  4:e2370.

6 Smallegange IM, and Coulson T (2013) Towards a general, population-level understanding of eco-evolutionary change. Trends in Ecology and Evolution 28: 143-148.

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