Phylogeny, competition and Darwin: a better answer?

*Sorry for the low frequency of posts these days – I seem to be insanely busy this summer ☺

Oscar Godoy, Nathan Kraft, Jonathan Levine. 2014. Phylogenetic relatedness and the determinants of competitive outcomes. Ecology Letters.

Ecology is hard in part because of the things we can’t (at least easily) measure: fitness, interaction strengths, and the niche, all fundamental ecological concepts. Since we are unable to measure these concepts directly, ecologists have come up with proxies and correlates. Take Darwin’s hypothesis that competition should be greater between closely related species. It relies a chain of assumptions about proxy relationships – first that relatedness should correlate with greater similarity of traits, secondly that similar traits should correlate with greater niche overlap. The true concept of interest, the niche, is un-measurable (if it is an n-dimensional hypervolume) so instead shared evolutionary history provides possible insight into species coexistence.

Ecophylogenetic studies have adopted Darwin's hypothesis as an example of how  molecular phylogenies may provide information about evolutionary history which in turn informs current ecological interactions. Phylogenies ideally capture feature diversity, and so (all things being equal) should provide information about similarity between species based on their relationship.  Despite this, studies have been mixed in terms of finding the relationship predicted by Darwin between phylogenetic relatedness and competition. It is not clear whether this mixed result suggests problems with the phylogenetic approaches being used, or non-generality of Darwin’s hypothesis.

Oscar Godoy, Nathan Kraft, and Jonathan Levine attempt to explore this question once again, but through the lens of Chesson’s coexistence framework (2000). Chesson’s framework describes competitive differences between species not as a single quantity, but instead the outcome of both stabilizing niche differences and equalizing fitness differences between species. This framework predicts that competitive differences should be greatest when species have similar niches (low stabilizing niche differences) and/or when they have large differences in fitness. This divisions alters the predictions from Darwin's hypothesis: if closely related species have similar niches, they should compete more strongly, but on the other hand, if closely related species have similar fitnesses, they should compete less strongly. Darwin’s hypothesis as it has been tested may be too simplistic.

The authors used an experiment involving 18 California grassland species to look at first, whether competitive ability is conserved, and more generally to explore whether phylogenetic distance predicts “the niche differences that stabilize coexistence and the fitness differences that drive competitive exclusion?” Further, can this information be used to predict the relationship between phylogeny and competitive outcomes? To determine this, they quantified germination, fecundity, seed survival, and interaction coefficients for the 18 species based on competition with different competitors (both by identity and density), and quantified the strength of stabilizing and equalizing forces (as in previous works). With this information, they calculated for each species the average fitness and ranked species in a competitive hierarchy using a fully parameterized annual plant population model. Species’ competitive rank did in fact show a phylogenetic signal (Figure 1), and the strongest competitors were clustered in the Asteraceae and its sister node.

Fig 1. Relationship between competitive rank among the 18 CA grassland species.

Competitive rank was then decomposed into fitness differences and niche differences. Fitness differences showed the clearest relationship with phylogeny - distantly related competitors had significantly greater asymmetries in fitness, closely related species had similar fitnesses (Figure 2). However stabilizing niche differences showed no phylogenetic signal at all (Figure 3, solid line).

Fig. 2. Relationships between fitness differences and phylogenetic distance.

Fig 3. Solid line - observed niche distances as a function of phylogenetic distance. Dashed line, size of distances actually needed to assure coexistence.

The authors could then calculate, for a given pair of species with a given phylogenetic distance, the expected fitness difference (based on the fitness difference-phylogeny relationship), and given this, the amount of stabilizing niche differences that would be necessary to prevent competitive exclusion between pairs of species. When they did this, they found that the required stabilizing niche differences were much larger than those that actually existed between the plants. This was especially true between distant related species(dashed line, Figure 3). Darwin’s hypothesis, that closely related species should be more likely to coexist, seemed to be reversed for these species.

How should we interpret these results more broadly? Is this reinforcement of the use of phylogenetic information to answer ecological questions, provided the questions are asked correctly? One of the most interesting contributions of this paper is their discussion of the oft-seen, but poorly incorporated, increase in variation in a trait (here fitness differences) as phylogenetic distances increase. This uneven variance often leads to phylogenetic-trait correlations being labelled non-significant, since it violates the assumptions of linear models. In contrast, here the authors suggest that this uneven variance is important. “For example, even if on average, both niche and fitness differences increase with phylogenetic distance, the increasing variance in these relationships means that only distant relatives are likely combine large competitive asymmetries with small niche differences (rapid competitive exclusion), or large niche differences with small competitive asymmetries (highly stable coexistence). Overall, our results suggest that increasing variance in niche or fitness differences with phylogenetic distance may play a central role in determining the phylogenetic relatedness of coexisting species.”

This discussion is important for questions about phylogenetic relatedness and coexistence – variability is part of the answer, not evidence against the existence of such relationships. However, a few caveats seem important: Because fitness differences and niche differences as defined in the Chesson framework may not be easily associated with traits (since a single trait might contribute to both components), it seems that it will be a little difficult to expand these analyses to less rigourous experimental settings. This might also be important to hypothesize how fitness or niche differences per se become associated with phylogenetic differences, since traits/genes are actually under selection. But the paper definitely provides an interesting direction forward.

Chesson, P. 2000. Mechanisms of maintenance of species diversity. Annual Review of Ecology and Systematics 31:343-366.