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

Why pattern-based hypotheses fail ecology: the rise and fall of ecological character displacement

Yoel E. Stuart, Jonathan B. Losos, Ecological character displacement: glass half full or half empty?, Trends in Ecology & Evolution, Available online 26 March 2013

Just as ecology is beginning to refocus on integrating evolutionary dynamics and community ecology, a paper from Yoel Stuart and Jonathan Losos (2013) suggests that perhaps the best-known eco-evolutionary hypothesis - Ecological Character Displacement (ECD) – needs to be demoted in popularity. They review the existing evidence for ECD and in the process illustrate the rather typical path that research into pattern-based hypotheses seems to be taking.

ECD developed during that period of ecology when competition was at the forefront of ecological thought. During the 1950s-1960s, Connell, Hutchinson and McArthur produced their influential ideas about competitive coexistence. At the same time, Brown and Wilson (1956) first described ecological character displacement. ECD is defined as involving first, competition for limited resources; second, in response, selection for resource partitioning which drives populations to diverge in resource use. Ecological competition drives adaptive evolution in resource usage – either resulting in exaggerated divergence in sympatry or trait overdispersion. ECD fell in line with a competition-biased worldview, integrated ecology and evolution, and so quickly became entrenched: the ubiquity of trait differences between sympatric species seemed to support its predictions. Pfennig and Pfennig (2012) go so far as to say ‘Character displacement...plays a key, and often decisive, role in generating and maintaining biodiversity.’

One problem was that tests of ECD tended to make it a self-fulfilling prophecy. Differences in resource usage are expected when coexisting species compete; therefore if differences in resource usage are observed, competition is assumed to be the cause. In the ideal test, divergent sympatric species would be found experimentally to compete, and ECD could be used to explain the proximal cause of divergence. But the argument was also made that when divergent sympatric species were not found to compete, this was also evidence of ECD, since “ghosts of competition past” could have lead to complete divergence such that competition no longer occurred. This made it rather difficult to disprove ECD.

There was pushback in the 1970s against these problems, but interestingly, ECD didn’t fall out of favour. A familiar pattern took form: initial ecstatic support, followed by critical papers, which were in turn rebutted by new experimental studies. Theoretical models both supported or rebutted the hypothesis depending on the assumptions involved. In response the large literature, several influential reviews were written (Schluter (2000), Dayan and Simberloff (2005)) that appeared to suggest at least partial support for the ECD from existing data. Rather than dimming interest in ECD, debate kept it relevant for 40+ years. And continued relevance translated to the image of ECD as a longstanding (hence important) idea. Stuart and Losos carry out a new evaluation of the existing evidence for ECD using Schluter and McPhail’s (1992) ‘6 criteria’, using both the papers from the two previous reviews and more recent studies. Their results suggest that strong evidence for ECD is nearly non-existent, with only 5% of all 144 studies meeting all 6 criteria. (Note: this isn't equivalent to suggesting that ECD is nearly non-existent, just that currently support is limited. There's a good discussion as to some of the possible reasons that ECD has been rarely observed, in the paper).

From Stuart and Losos (2013). Fraction of cases from Schluter 2000, Dayan and Simberloff 2005, and this study that meet either 4 or all 6 of the criteria for ECD.

The authors note that there are many explanations for this finding of weak support: the study of evolution in nature is difficult, particularly given the dearth of long term studies. The 6 criteria are very difficult to fulfill. But they also make an important, much more general point: character displacement patterns can result from multiple processes that are not competition, so patterns on their own are not indicative. Patterns that result from legitimate ecological character displacement may not show the predicted trait overdispersion. The story of the rise and fall of ECD is a story with applications to many pattern-driven ecological hypotheses. There are many axiomatic relationships you learn about in introductory courses: productivity-diversity hump shaped relationships, the intermediate disturbance hypothesis, ECD, etc, etc. These have guided hypothesis formation and testing for 40 years and have become entrenched in the literature despite criticism. And similarly, there are recent papers suggesting that long-standing pattern-based hypotheses are actually wrong or at least misguided (e.g. 1, 2, 3, etc). Why? Because pattern-driven hypotheses lack mechanism, usually relying on some sort of common-sense description of a relationship. The truth is that the same pattern may result from multiple processes. Further, a single process can produce multiple patterns. So a pattern means very little without the appropriate context.

So have we wasted 40 years of time, energy and resources jousting at windmills? Probably not, data and knowledge are arrived at in many ways. And observing patterns is important - it is the source of information from natural systems we use to develop hypotheses. But it is hopeful that this is a period where ecology is recognizing that pattern-based hypotheses (and particularly the focus on patterns as proof for these hypotheses) ask the right questions but focus on the wrong answers.

Long-term studies of Darwin's finches have provided strong evidence for ECD.