Pleiotropy allows the evolutionary maintenance of positive niche construction in the face of free-riders
7 May 2018
In our paper published recently in American Naturalist, we used mathematical models to help us understand how positive niche construction can be maintained. Many animals, plants and other organisms engage in niche construction, that is, they modify the environment and the subsequent selective pressures to which they are exposed. Positive niche construction occurs when organisms modify the environment to their advantage; for example, beavers create dams to provide shelter and other benefits. So-called free-riders can emerge who don’t contribute to the costly niche construction but still benefit from the niche-constructing activities of others. This raises an evolutionary problem of how positive niche construction can emerge and be maintained if it is constantly challenged by free-riders.
Work from biology and economics has shown that niche construction can be maintained if free-riders are excluded from the constructed niche or resource. One way to do this is if niche constructors and their offspring can monopolize the constructed resource, such as in the case of social spiders and their constructed webs. Similarly, burrowing animals naturally exclude other individuals by immediately occupying the burrows they create. Exclusion of free-riders can thus be achieved through strong spatial structure, and also through punishment of free-riders, or kin selection, where transgenerational inheritance favors the offspring and other relatives of niche constructors.
Because these mechanisms of exclusion can become separated from the ability to construct the niche, they still allow the emergence of free-riders and are therefore only a partial explanation for the persistence of positive niche construction. In our paper, we discuss a different mechanism to exclude free-riders: that niche constructors are (or become) better-adapted to the constructed environment than free-riders. For example, niche constructors may be better or more efficient at utilizing the resource they create. This could be manifest in the ability of spiders to defend their webs against other spiders, or the ability of birds to defend their nests against nest parasites, for example. We call this mechanism resource adaptation.
Even in this scenario, free-riders who become highly resource-adapted but don’t contribute to niche construction can still appear. However, if the two traits – niche construction and resource adaptation – are inextricably linked, then niche construction could emerge and persist. This could be an inseparable link between niche construction and a benefit that is unavailable to free-riders, or it could be an inseparable link between free-riding and an additional cost that is not paid by niche constructors. We hypothesize that pleiotropy (when one gene influences more than one trait) could be responsible for linking the niche construction and resource adaptation traits. If the same genes or functions that contribute to niche construction abilities also contribute to being able to capitalize on the results of that niche construction, free-riding becomes costly and niche construction can be maintained.
We evaluated our hypothesis using mathematical models. First, we presented a phenotypic model of niche constructing organisms, where organisms modify the environment to differing degrees, utilize the constructed environment/resource in different ways, and compete with each other for access to the constructed resource. Importantly, niche construction comes at a fitness cost to individuals. We used our model to investigate population- and evolutionary- dynamics in different scenarios.
If all organisms are equally adapted to the resource, then those who contribute least to niche construction incur the lowest fitness cost and out-compete the niche constructors. But what happens when some organisms are better adapted to the constructed resource than others? We started with a population where the niche-construction trait was fixed and the environmental resource was at equilibrium. We then allowed the introduction of rare mutants, with altered niche constructing abilities and resource adaptation. In this model, the two traits were allowed to evolve independently. We found that niche construction was only transiently maintained because free-riders, who were highly adapted to the resource but didn’t contribute to the niche construction, took over.
Next, we considered the scenario where a trade-off exists between the two traits. For example, free-riding could come at the cost of reduced resource adaptation. Alternatively, the costly activity of niche construction could come with the additional benefit of greater adaptation to the constructed resource. This trade-off could lead to positive evolutionary feedback, leading to a further-improved environment and a better resource-adapted organism. For this to happen, the positive relationship between niche construction and resource adaptation would have to be sufficiently strong (or the cost to free-riders sufficiently high) to prevent the appearance of free-riding mutants.
We went back to our model but this time the mutants that were introduced into the otherwise stable system were different: changes in the niche construction trait were positively correlated with changes in the resource adaption trait such that better niche constructors were also better adapted to using the constructed resource. Repeating the simulations, we found that niche construction was maintained over evolutionary time when the correlation between the two traits was sufficiently strong. In other words, the amount of niche construction increased over evolutionary time when the fitness gain due to better resource adaptation (relative to the associated change in niche construction) outweighed the cost of niche construction.
Having shown that a trade-off between a niche construction trait and another trait that compensates for the cost of niche construction can prevent the emergence of free-riders, we wanted to understand how this might occur mechanistically. We considered genetic mechanisms. If there is a gene for each trait, close physical linkage (when the genes are next to each other on the chromosome) may result in a transient correlation, but they would eventually become independent through recombination or mutation. If, however, a single gene controlled both the niche construction trait and the resource adaption trait, the two would stay correlated. This pleiotropy would mean that when niche construction ability is lost, so too is the ability to utilize the constructed resource.
To investigate this in light of our results above, we used a population-genetics model with two genes (or loci). In the simplest case, when each gene controlled a single trait, niche construction was lost due to the appearance of free-riders. However, we identified scenarios where positive niche construction was maintained over evolutionary time. We introduced (i) pleiotropy, where the first gene controlled both niche construction and the ability to utilize the constructed niche and (ii) epistasis, where a second gene interacted with the first gene to contribute to the resource adaptation trait. When the pleiotropy, epistasis, or a combination of the two were strong enough, positive niche construction was maintained.
In fact, we found that the second gene wasn’t even needed in order to maintain positive niche construction, if the pleiotropic effect of the first gene (on the ability to niche construct and utilize the constructed niche) alone outweighed the cost of niche construction. This means that pleiotropy can indeed promote the evolutionary maintenance of positive niche construction, by coupling it with other beneficial effects to prevent the appearance of free-riders.
For more detail, read the paper here:
Chisholm RH, Connelly BD, Kerr B, Tanaka MM. 2018. The role of pleiotropy in the evolutionary maintenance of positive niche construction. Am Nat DOI: 10.1086/697471.