Wednesday, July 22, 2015

Habitat preference and speciation

Back in 2006, during my field work on Vancouver Island for my postdoc project with Andrew Hendry on threespine stickleback in contiguous lake and stream habitats, I was deeply impressed by the phenotypic differentiation these populations exhibit across extremely steep ecological transitions – often without any obvious physical dispersal barrier. For example, the left picture below shows the abrupt transition from Robert’s Lake (background) into its outlet stream (foreground). Morphological divergence between these populations was immediately obvious in the field (right picture: adult stream male on top, adult lake male below), and analyzing microsatellite data later showed that phenotypic divergence was paralleled by equally striking genetic shifts (for details see Berner et al. 2009, Evolution). This made me really think about what reproductive barrier(s) could maintain such steep divergence in the face of dispersal opportunities, and my intuition was that perhaps lake and stream fish simply wanted to stay in their native habitats, rather than disperse.

In the same period and in the same study region, Dan Bolnick and his crew performed a very cool field experiment: they sampled stickleback from a lake and its inlet stream, marked the sampled fish according to the habitat in which they had been found, released them in the habitat transition, and checked where they then dispersed by re-capture. Put simply, this experiment made clear that each population preferred to return into its original habitat (Bolnick et al. 2009, Evolution).

Inspired by these observations, I felt that theory was needed to explore how habitat preference can promote adaptive divergence and speciation. Of course, a great deal of theory was already available demonstrating that many forms of non-random dispersal can promote divergence, but this evidence seemed rather scattered and often disconnected from biologically realistic contexts. Hence I started a large-scale simulation project with Xavier Thibert-Plante, a theoretician and friend I got to know in Montreal during my postdoc with Andrew. This work was initially tailored to parapatric lake-stream stickleback, but then we abandoned that specific context in favor of a broader study. Our simulation study considers the scenario in which two populations diverge in the face of gene flow, allowing for the simultaneous evolution of ecological adaptation and dispersal modification. This dispersal modification is modeled to arise from several different habitat preference mechanisms, including habitat imprinting during the juvenile stage, phenotype-dependent habitat preference, or a genetically hard-wired preference for a certain habitat type. We felt that this diversity in the mechanisms underlying habitat preference was crucial, because in natural systems where habitat preference has been inferred, the proximate cause of habitat preference is often not clear.

We find that habitat preference will often evolve so as to reduce gene flow between the habitats. This works best and promotes adaptive divergence most effectively when gene flow between the populations is initially substantial – a domain where migration–selection balance under random dispersal permits weak divergence only. This makes habitat preference a particularly relevant factor in the early stages of speciation when other reproductive barriers are still weak or absent. Comparing the different habitat preference mechanisms further reveals that speciation is strongly facilitated by habitat imprinting, whereas mechanisms like direct genetic preference or pure density-dependence are ineffective contributors to divergence. Moreover, we find that divergence with habitat preference is influenced by asymmetry in the size of the diverging populations, and by variation in the number of genetic factors encoding the simulated traits. Overall, our study indicates that habitat preference deserves much wider recognition when studying the divergence and reproductive isolation of populations. If interested, see Berner & Thibert-Plante 2015, J. Evol. Biol. in press.


The figure above is taken from the paper and shows the evolution of habitat preference via an imprinting trait (upper row), and the facilitation of adaptive divergence by this mechanism relative to random dispersal (bottom row), across combinations of the strength of divergent selection and initial dispersal.  (Click image to see at larger size.)

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