Because more closely related species often share ecologically-important traits, ecologists initially predicted that competitive exclusion would occur more frequently between recently diverged species1. In nature, however, phylogeny-coexistence relationships are often weak at best, or lack generality2. Most work attributes this apparent disconnect between theory and reality to the lack of conservatism in the underlying traits3.

An additional but rarely examined problem is that trait differences can both promote (niche differences) and deter (fitness differences) coexistence (fig. 1). As such, closely related species can be either more or less likely to coexist, depending on the relative strength of niche and fitness differences4. However, it remains unknown what determines the relative strength niche versus fitness differences and how these differences contribute to phylogeny-coexistence relationships.

Biogeographic history may shape the evolutionary trajectories of niche and fitness differences between species. When competitors originate from the same biogeographic region, niche differences should evolve faster than fitness differences (fig. 2A) to explain the high diversity in nature, and promote coexistence between more distantly related species. This is possible because competition is a well-known driver of niche divergence between co-occurring species5, but may simultaneously cause species to become more similar than different in fitness as poor competitors are excluded from the community. When competitors originate from different biogeographic regions, rates of niche divergence are unpredictable with respect to evolutionary relationships, with the potential for fitness differences to accumulate and drive

Evolution of species interactions in Mediterranean annual plant communities

Rachel M. Germain and Benjamin Gilbert; Dept. of Ecology & Evolutionary Biology, University of Toronto

Experimental workBackground Biogeographic history influences species interactions

Figure 3. Population dynamics of exotic species (orange) when introduced to a native community (black) in a new region, according to four scenarios: (A) no niche or fitness differences, (B) no niche but fitness differences, (C) niche but no fitness differences, and (D) both niche and fitness differences. Dashed lines in drawing represent distinct spatial niches. Plant drawings modified from F. L. Pérez 2011.

ACKNOWLEDGMENTS

competitive exclusion6,7 (fig. 3B,D). This latter phenomenon is the product of differences both in the underlying environmental conditions and in community-wide fitness among species in their home and introduced ranges. For example, the invasion of European grasses across California landscapes has been attributed to the long history of grazing pressure in their home range8, selecting for traits that accelerate growth and provide a competitive advantage in regions where grazing pressure is relaxed. The unpredictability associated with species from different biogeographic regions is consistent with observed patterns of species invasions, where some species have spectacularly negative impacts on native diversity while others fail to invade altogether9.

How do species differences and biogeography combine to regulate phylogeny-coexistence relationships?

Study system

• 32 species native to the mediterranean grasslands of California or Spain, selected to capture a wide range of the taxonomic diversity found in both regions

Experimental setup

• Greenhouse experiment (fig. 4) from January to August 2012

• Niche differences: plants grown at a constant density at six frequencies of species A to species B

• Fitness differences: each species grown alone at low densities to estimate seed production in the absence of competition

• Mathematical models are used to compare the population growth rates (estimated via seed production) when competitors originate from the same and different biogeographic regions

I predict that stable coexistence should occur more frequently between distantly related species that have coevolved through evolutionary time (fig. 2A).

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Although most contemporary work acknowledges that niche and fitness differences both contribute to species coexistence, their evolutionary trajectories and corresponding implications for community structure remain unknown. Trait differences should be minimal immediately after speciation, and increase over evolutionary time as species diverge (fig. 2). Because it seems unlikely that niche and fitness differences evolve at the same rate, the probability of coexistence can either increase (fig. 2A) or decrease (fig. 2B) over evolutionary time depending on which trait-type evolves faster.

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Figure 1. Trait differences can both promote (left) and deter (right) coexistence. The 1:1 line indicates the boundary between positive and negative population growth in one time step.

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Figure 2. Evolutionary trajectories of niche (α) to fitness (λ) differences and corresponding implications for species coexistence. In scenario A, coexistence occurs because niche differences evolve faster than fitness differences (i.e., Δα/Δλ > 1). In scenario B, exclusion occurs because niche differences evolve slower than fitness differences (i.e., Δα/Δλ < 1).

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References: 1. Elton CS, 1946, J. of Anim. Ecol. 15: 54-68; 2. Swenson NG, Enquist BJ, 2009, Ecology 90: 2161-2170; 3. Cavender-Bares J, Keen A, Miles B, 2006, Ecology 87: S109-122; 4. Mayfield MM, Levine JM, 2010, Ecol. Lett. 13: 1085-1093; 5. Dayan T, Simberloff D, 2005, Ecol. Lett. 8: 875-894; 6. MacDougall AS, Gilbert B, Levine JM, 2009, J. of Ecol. 97: 609-615; 7. Strauss SY, Webb CO, Salamin N, 2006, PNAS 103: 5841-5845; 8. Mitchell CE, Agrawal AA, Bever JD, Gilbert GS, Hufbauer RA, Klironomos JN, Maron JL, Morris WF, Parker IM, Power AG, Seabloom EW, Torchin ME, Vazquez DP, 2006, Ecol. Lett. 9: 726-740; 9. Williamson M, Fitter A, 1996, Ecology 77: 1661-1666.

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Figure 4. Photos of greenhouse experiment, which includes 16 species pairs that span a broad range of divergence times and originate from either the same or different biogeographic regions.