Reproductive Character Displacement or Alternative Explanations?

*Guest post by Santiago J. Sánchez-Pacheco

Closely related animal species are often so similar that it is hard to distinguish them. This immediately leads to the question of how the individuals of such species, when in sympatry, can recognize their conspecifics. Usually, the species differ in traits (i.e., species recognition signals; e.g., visual and sound signals) that are detectable by sensory mechanisms. Less is known, however, about how these phenotypic differences evolve. A common view is that hybrids suffer reduced fitness or cannot be produced whatsoever, and therefore selection should favor individuals with traits that avoid interspecific matings. By diverging in such traits, females and males of closely related species are less likely to waste energy in failed matings. This widely accepted assumption is usually referred to as “reproductive character displacement” (Losos, 2013).  

From Evolution (Third edition; Futuyma, 2013).

When Brown and Wilson (1956) described character displacement, they proposed the following process: populations of two closely related species, after first coming into contact with each other, interact “in such a way as to diverge further from one another where they occur together”. Such divergence minimizes the chances of both competition and hybridization between the species, and therefore favors coexistence over exclusion.

While it is generally accepted that natural selection is the force increasing the frequency of the divergent traits, whether or not the resulting divergence is driven by the interaction between the two species (e.g., competition) remains uncertain. If a pattern of differences is consistently detected between populations of two closely related species when they are compared in allopatry versus sympatry, it seems reasonable to attribute this pattern to the interaction of both species. However, a number of processes other than a response to interspecific interaction may result in a “displacement-like” pattern—substantial differences of the environments between allopatry and sympatry, phenotypic plasticity or even random processes can all trigger differentiation (Kamath, 2014).   

Based on six criteria (Box 1) established by Schluter & McPhail (1992) as general indicators to rule out alternative processes that might lead to a displacement-like pattern, recently Stuart & Losos (2013) pointed out that only a small portion (9 of 144 cases) of recent studies claiming evidence for ecological character displacement can conclude with a high degree of certainty that the interspecific interaction led to the observed divergence. According to Stuart & Losos, falsification of only one of these six criteria is enough evidence to determine that such divergence did not result from character displacement. Consequently, their findings suggest that most documented cases of ecological character displacement are equally consistent with other evolutionary and ecological phenomena. Although these two studies focus only on ecological character displacement, it is worth noting that the same eco-evolutionary principles underlie reproductive character displacement, so that alternative processes could also explain phenotypic differentiation presumably derived from interspecific interaction.

Despite the concept of character displacement having remained in the evolutionary literature for decades, this assumption has seldom been subjected to critical scrutiny. Indeed, it was not until recently that significant progress in designing thorough studies to rigorously test this adaptive hypothesis was achieved (e.g., Stuart et al. [2014]).

Box 1: Modified from Stuart and Losos (2013). The six criteria for Ecological Character Displacement (ECD).

References

Brown Jr., W. L. and E. O. Wilson. 1956. Character displacement. Systematic Zoology 5(2): 49–64.

Kamath, A. 2014. http://www.anoleannals.org/2014/10/25/rapid-evolution-in-anolis-carolinensis-following-the-invasion-of-anolis-sagrei/

Losos, J. 2013. http://www.anoleannals.org/2013/08/12/reproductive-character-displacement-and-dewlap-color-in-haitian-anoles/

 

Schluter, D. and J. D. McPhail. 1992. Ecological character displacement and speciation in sticklebacks. The American Naturalist 140: 85–108.

Stuart Y. E. and J. B. Losos. 2013. Ecological character displacement: glass half full or half empty. Trends in Ecology and Evolution 28(7): 402–408.

Stuart Y. E., Campbell T. S., Hohenlohe, P. A., Reynolds, R. G., Revell, L. J. and J. B. Losos. 2014. Rapid evolution of a native species following invasion by a congener. Science 346: 463–466.

A blog post reviewing Stuart and Losos (2013) from a different perspective:

http://evol-eco.blogspot.ca/2013/05/why-pattern-based-hypotheses-fail.html

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.

Competition and mutualism may be closely related: one example from myrmecochory

Robert J. Warren II, Itamar Giladi, Mark A. Bradford 2014. Competition as a mechanism structuring mutualisms. Journal of Ecology. DOI: 10.1111/1365-2745.12203.

As ecologists usually think about them, competition and mutualism are very different types of interactions. Competition has a negative effect on resource availability for a species, while mutualism should have a positive impact on resource availability. Mutualisms involve interactions between two or more species, and as such are biotic in nature. While the typical definition of the fundamental niche includes all (and only) abiotic conditions necessary for a population’s persistence, with the realized niche showing those areas that are suitable once biotic interactions are considered (Pulliam 2000), mutualisms are a reminder that the a niche is not as simple as we hope. Mutualisms may be necessary for a population’s persistence, as in the case of obligate pollinators, and so some biotic interactions might be “fundamental”. More complicated still, species may compete for mutualist partners – plant species for pollinators, for example. If the mutualist partner is considered a resource, mutualism and competition may not be so far apart after all. 

The relation between competition and mutualism is probably most acknowledged in terms of pollinators – patterns of staggered flowering in a plant community arise in part to decrease simultaneous demand for limited pollinator resources. Another possibly fundamental biotic resource is dispersers, which may be necessary for population persistence of some species. In Warren, Giladi, and Bradford (2014), the authors attempt to expand this idea of competition for mutualist partners to ant-mediated seed dispersal or myrmecochory. Myrmecochorous plant species are common in a number of regions of the world. They rely on ant dispersal to move their seeds, helping to increase the distance between parent and offspring (and thus decrease competition), lower seed predation, and introduce seeds to novel habitats. Ant species that disperse these seeds benefit from the high-energy seed attachment (elaiosome) provided by the plant. While myrmecochorous plants are dependent on ants for successful dispersal, most ants do not rely solely on elaiosomes for food; further, there are fewer seed-dispersing ant species than there are ant-requiring plant species. As a result, competition for ants between myrmecochorous species is a reasonable hypothesis. If there is competition for mutualist partners, the predictions are that species either increase their attractiveness as a competitor by making their seeds most attractive, or else decrease the intensity of competition by staggering seed release.

Warren et al. tested this predictions for eastern North American woodland perennials: at least 50 plant species rely on ant dispersal in this region, but a much smaller number of ants actually disperse seeds. This dearth of mutualist partners implies that competition for ant dispersers should be particularly strong. One way to successfully monopolize a mutualist is to ensure that the timing of seed release is coordinated with ant availability and attraction: in fact comparisons between myrmecochorous and non-myrmecochorous plant species suggests that those requiring ants set seed earlier, when ant attraction to seeds is higher (insect prey become more attractive later in the season). To look at competition within myrmecochorous species, the authors as whether seed size (and thereby attractiveness to ants) was staggered through time. Smaller mymecochore seeds should, for example, become available when larger and more attractive seeds are not in competition. This prediction held – small, less attractive seeds were available earlier in the season than the larger, more attractive later seeds. The authors then experimentally tested whether small and large seeds were in competition for ants and differed in their success in attracting them. Using weigh boats secured to the forest floor, the researchers provided either i) only small myrmecochore seeds, ii) only large seeds, or iii) a combination of both seed sizes. Not that surprisingly, the presence of large seeds inhibits the removal of smaller less attractive seeds by as much as 100% (i.e. no small seeds were removed).

The authors do a nice job of showing that species differ in their success in attracting ant dispersers, and species with differing seed attractiveness appear to partition the season in such a way as to maximize their success. Whether or not this likely competition for dispersers extends to impact the species’ spatial distribution or whether species are prevented from co-occurring by competition for mutualists is less clear, and an interesting future direction. The authors also hypothesize that dispersers, rather than pollinators, may drive flowering/seed production in a system, which is an alternative the usual assumption that pollinators, not dispersers are more important drivers of evolution. More generally, the paper is a reminder that, at least for some species, biotic interactions are fundamental to the niche. Or even more likely, that the separation between the determinants of a fundamental and realized niche aren’t so very distinct. And that’s a reminder that has value for many sections of ecology, from species distribution models to invasive species research.

Evidence for the evolution of limiting similarity in diving beetle communities

Remi Vergnon, Remko Leijs, Egbert H. van Nes, and Marten Scheffer. (2013) Repeated Parallel Evolution Reveals Limiting Similarity in Subterranean Diving Beetles. The American Naturalist, Vol. 182, pp. 67-75.

In 2006, Marten Scheffer and Egbert van Nes published a very nice paper showing the outcome of simulated evolution of competing species. Their results showed how patterns of evenly-spaced clusters of species along a niche axis could evolve to minimize competition via limiting similarity. 

From Scheffer and van Nes (2006): Evenly spaced clusters of species along a niche axis (x-axis) evolved in response to competition.

Within any cluster along the niche axis, species tended to be more similar than expected. The results suggested that complex self-organizing clustered patterns might result from simple competitive limitations. Interestingly, although the original paper suggested that clustered patterns in size distributions are common, only now are these theoretical expectations about the evolution of limiting similarity being tested with data. In fact, though theory has long suggested that patterns of limiting similarity should evolve to allow coexistence between competing species, empirical evidence is rather lacking. Despite this, limiting similarity and competition are staples of ecological thought: for example, patterns of overdispersion in traits or relatedness are often used as evidence for the importance of competition.

The follow-up paper -Vergnon et al. (2013)- tests for the pattern predicted in Scheffer and van Nes (2006) using communities of subterranean diving beetles (Coleoptera, Dytiscidae) in Australia. These species have evolved for over 5 million years in isolated aquifers. If limiting similarity structured beetle communities, the authors predicted that there should be regularity in the spacing of species along a niche axis. If competitive interactions determine species' positions on the niche axis, then their absolute positions on the niche axis could vary between communities so long as their relative positions are evenly spaced. If, in contrast, niches are driven by environmental conditions, species in different communities/aquifers should have similar absolute positions along the niche axis.

The authors used a nice combination of statistics, modelling and observational data (34 communities of beetles representing 75 total species) to test for these predicted patterns. They used beetle size as the measure of niche position, since size is often an indicator of niche position and food availability and identity. For almost all aquifers, co-occurring beetles were significantly different in size. Further, species in different aquifers classified as occurring in the same size classes (small, medium, large), had different absolute sizes (i.e. the largest beetle in one 2-species aquifer was not similar in size to the largest beetle in another 2-species aquifer).  

From Vergnon et al. (2013): Absolute sizes of diving beetles in aquifers with 3 species present. The absolute size in a size class (large - black; medium - white; small - grey) varies between aquifers.

Although the absolute size of species differed between aquifers, the ratio of sizes (regularity of spacing on the niche axis) was highly consistent. Further, simulations of evolution of body size due to competition were capable of reproducing the observed size structure of the diving beetles.

From Vergnon et al. (2013): regularity of spacing between competing diving beetles (measured as the body size ratio). 

This paper does a nice job of integrating theory and data, and combining pattern and process. The focus is on testing contrasting predictions, and the authors use complementary approaches to test statistically for the presence of patterns and to demonstrate with simulations the relationship between the evolution of limiting similarity and the observed pattern. The evidence is suggestive that limiting similarity and not pre-existing environmental niches explains the size structure of communities of competing diving beetles. There are still questions about how far these inferences can be extended. For example, do we expect that predefined environmental niches are really the same across aquifers? How important is competition in these communities - at the moment, the authors only have minimal evidence of gut content overlap from a single aquifer. Further the low diversity of aquifer communities (~1-5 diving beetle species) means that the prediction of clusters of multiple similar species made in the original Scheffer and van Nes paper can't be tested. But the fact that aquifer diving beetle communities have low diversity and are very simplistic is beneficial for the authors. Patterns in diverse communities where multiple processes (predation, migration, etc) are important may be too complex to show clear evidence in observational data. Simple systems (including microcosms) are a good place to find evidence that a process of interest actually occurs. Whether or not that process is important across many systems is of course a more difficult question to answer.