Habitat-matching dispersal facilitates local adaptation

Migration disrupts local adaptation. At least, this is the first reaction I have when I consider these two processes. In fact, my initial thought is almost always: how strong does selection have to be to overcome gene flow? Gene flow can work to diminish adaptation by swamping out locally adapted alleles and homogenizing populations. Depending on the level of gene flow, selection may have to be quite strong to prevent the swamping of adaptive alleles. This line of thinking is, of course, too simplistic (For a review of gene flow and local adaptation, see Tigano and Friesen 2016).
First, gene flow can provide a source of adaptive genetic variation, known as adaptive introgression; think Heliconius butterflies. Secondly, migration and gene flow aren’t necessarily random. That is, individuals may preferentially migrate to habitats where their fitness is maximized. This can lead to adaptation instead of inhibiting it. This latter point is one I think is commonly overlooked and goes by names including habitat-matching dispersal, phenotypic sorting, matching habitat choice, directed movement, phenotype-dependent dispersal, and others (See Edelaar et al., 2008 for a good overview of the topic.). Habitat-matching dispersal can work to facilitate rather than hinder adaptation and is has a very different effect on adaptation than random dispersal.

While habitat choice may be an important process in local adaptation, there has been little experimental validation of this idea. In their recent paper, Jacob and colleagues used the ciliate Tetrahymena thermophile to test effects of random versus directed migration on adaptation to high temperature.

Figure 1 from Jacob et al. 2017. Red points are cells that stay or move to the high temperature environment, blue the low temperature environment, and grey had no migration opportunity

The authors first demonstrated that these cells actively choose (or stay in) habitats that maximize their fitness. Three treatments were used: 1) Non-dispersal where cells were placed in 23 or 35°C with no migration opportunity; 2) Habitat choice where cells started at 23°C and could migrate to 23 or 35°C; 3) Habitat choice where cells started at 35°C and could migrate to 23 or 35°C. Cells that chose to migrate or stay in the 35°C habitat showed higher growth at 35°C than those that didn’t (see figure 1).
Following this, the authors looked at the effect of directed versus random migration on adaptation to 35°C. A selection experiment was run for 6 weeks (~250 generations) at 35°C where each week cells from the above described habitat choice experiment were introduced as migrants. That is, cells that chose or stayed at 23°C, cells that chose or stayed at 35°C, and cell that had no habitat choice (this is the random dispersal group).

Figure 2 from Jacob et al. 2017. Note that growth rate with migrants choosing high temperature significantly increased (red/orange lines) while all other lines showed no increase or decreased growth.

The results show clearly that habitat matching dispersal facilitated adaptation to high temperature (see figure 2). While there is some variation in the responses, these results hold even for those individuals that chose to stay at 35°C, suggesting that this pattern isn’t simply driven by high fitness of well dispersing cells. Importantly, the groups receiving random dispersal did not adapt to high temperature, supporting the classic idea that gene flow can swap out locally adapted alleles.
I think this experiment did an excellent job testing an important process of adaptation that I had not previously given much thought. The findings are well summarized by the authors.

Our study demonstrates how the behaviours underlying dispersal—random versus active habitat choice movement—can shift the effects of gene flow from constraining to facilitating local adaptation. Habitat choice should drastically increase a species’ ability to adapt to new environmental conditions, especially compared with expectations from current models on the consequences of climate change, which largely assume random dispersal.

Edelaar, P., Siepielski, A.M. and Clobert, J., 2008. Matching habitat choice causes directed gene flow: a neglected dimension in evolution and ecology. Evolution62(10), pp.2462-2472.
Jacob, S., Legrand, D., Chaine, A.S., Bonte, D., Schtickzelle, N., Huet, M. and Clobert, J., 2017. Gene flow favours local adaptation under habitat choice in ciliate microcosms. Nature Ecology & Evolution1, pp.1407-1410.
Tigano, Anna, and Vicki L. Friesen. “Genomics of local adaptation with gene flow.” Molecular ecology 25, no. 10 (2016): 2144-2164.

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