Ecological and community-wide character displacement: the next generation

Ecological character displacement, mostly seen as increased differences of size in sympatry between closely‐related or similar species, is a focal hypothesis assuming that species too similar to one another could not coexist without diverging, owing to interspecific competition. Thus, ecological character displacement and community‐wide character displacement (overdispersion in size of potential competitors within ecological guilds) were at the heart of the debate regarding the role of competition in structuring ecological communities. The debate has focused on the evidence presented in earlier studies and generated a new generation of rigorous, critical studies of communities. Character displacement research in the past two decades provides sound statistical support for the hypothesis in a wide variety of taxa, albeit with a phylogenetically skewed representation. A growing number of studies are strongly based in functional morphology, and some also demonstrate actual morphologically related resource partitioning. Phylogenetic models and experimental work have added to the scope and depth of earlier research, as have theoretical studies. However, many challenging ecological and evolutionary issues, regarding both selective forces (at the inter‐ and intraspecific level) and resultant patterns, remain to be addressed. Ecological character displacement and community‐wide character displacement are here to stay as the focus of much exciting research.     

Ecological character displacement caused by reproductive interference

We carried out a theoretical investigation of whether ecological character displacement can be caused by reproductive interference. Our model assumes that a quantitative character is associated with both resource use and species recognition, and that heterospecific mating incurs costs. The model shows that ecological character displacement can occur as a consequence of evolution of premating isolation; this conclusion is based on the premise that resource competition is less intense between species than within species and that the ecological character also contributes to premating isolation. When resource competition between species is intense, extinction of either species may occur by competitive exclusion before ecological character divergence. Some observational studies have shown that character displacement in body size is associated with not only resources use but also species recognition. We propose that body size displacement can occur as a consequence of evolution of premating isolation. Our results suggest that ecological character displacement results from reproductive character displacement.     

Convergent and divergent character displacement

Consideration of the possibilities and difficulties of detecting character displacement leads to a re-definition of the phenomenon; character displacement is the process by which a morphological character state of a species changes under Natural Selection arising from the presence, in the same environment, of one or more species similar to it ecologically and/or reproductively. This incorporates the principal ideas in the original definition given by Brown & Wilson (1956), but eliminates the restriction of making comparisons of the character states of a species in sympatry and allopatry. The evidence for the ecological (competitive) aspect of character displacement is assessed by analyzing in detail the best documented and well publicized examples in the literature. Some of the examples either do not exhibit displaced characters or, if they do, the “displacement” can be interpreted in other and perhaps simpler ways; this applies to the so-called classical case of character displacement, Sitta tephronota and S. neumayer in Iran. Other examples, involving lizards and birds, constitute better evidence for character displacement, but in no single study is it entirely satisfactory. It is concluded that the evidence for the ecological aspect of character displacement is weak.     

Species co-existence and character divergence across carnivores

Co-occurring species might be morphologically similar because they are adapted to the same environment, or morphologically dissimilar to minimize competition. We use sister species comparisons to evaluate the relationship between morphological disparity and regional patterns of co-occurrence across carnivores. Up to 63% of the variation in range overlap can be explained by morphological divergence in dentition. Species that differ more in carnassial tooth length overlap more in their geographical range. Carnassials are the primary teeth associated with food processing, and hence difference in carnassial size may be a good indicator of difference in resource use. We suggest this pattern is consistent with competition in sympatry driving ecological character displacement, or competitive exclusion among ecologically similar species. Our study uses newly available data on global distributions, morphology and phylogeny, and is the first to demonstrate a close relationship between morphological disparity and co-occurrence at a regional scale encompassing multiple communities.     

The case for character displacement in plants

The evidence for character displacement as a widespread response to competition is now building. This progress is largely the result of the establishment of rigorous criteria for demonstrating character displacement in the animal literature. There are, however, relatively few well-supported examples of character displacement in plants. This review explores the potential for character displacement in plants by addressing the following questions: (1) Why aren''t examples of character displacement in plants more common? (2) What are the requirements for character displacement to occur and how do plant populations meet those requirements? (3) What are the criteria for testing the pattern and process of character displacement and what methods can and have been used to address these criteria in the plant literature? (4) What are some additional approaches for studying character displacement in plants? While more research is needed, the few plant systems in which character displacement hypotheses have been rigorously tested suggest that character displacement may play a role in shaping plant communities. Plants are especially amenable to character displacement studies because of the experimental ease with which they can be used in common gardens, selection analyses, and breeding designs. A deeper investigation of character displacement in plants is critical for a more complete understanding of the ecological and evolutionary processes that permit the coexistence of plant species.     

Parallel evolution and ecological selection: replicated character displacement in spadefoot toads

Ecological character displacement—trait evolution stemming from selection to lessen resource competition between species—is most often inferred from a pattern in which species differ in resource-use traits in sympatry but not in allopatry, and in which sympatric populations within each species differ from conspecific allopatric populations. Yet, without information on population history, the presence of a divergent phenotype in multiple sympatric populations does not necessarily imply that there has been repeated evolution of character displacement. Instead, such a pattern may arise if there has been character displacement in a single ancestral population, followed by gene flow carrying the divergent phenotype into multiple, derived, sympatric populations. Here, we evaluate the likelihood of such historical events versus ongoing ecological selection in generating divergence in trophic morphology between multiple populations of spadefoot toad (Spea multiplicata) tadpoles that are in sympatry with a heterospecific and those that are in allopatry. We present both phylogenetic and population genetic evidence indicating that the same divergent trait, which minimizes resource competition with the heterospecific, has arisen independently in multiple sympatric populations. These data, therefore, provide strong indirect support for competition''s role in divergent trait evolution.     

Guild composition and mustelid morphology – character displacement but no character release

Aim  Competition is hypothesized to lead to the evolution of reduced morphological overlap between competitors. Within guilds, this is believed to lead to overdispersed size ratios of the trophic apparatus of adjacent-sized species. In allopatry, conditions are believed to favour character release. We examined whether character displacement is prevalent in mainland musteline guilds and sought evidence for character release in adjacent island guilds.
Location  Holarctic, from Japan through western Europe to Pacific North America.
Methods  We measured skulls and canines of members of the mustelid subfamily Mustelinae and examined whether size ratios tend towards equality. We then examined whether insular guilds are characterized by larger size ratios and a higher degree of sexual size dimorphism than mainland guilds, and whether this reflects evolution towards the size of missing guild members.
Results  We found equal ratios between skull lengths but not canine diameters in all mainland guilds. Few insular guilds showed equal ratios for either trait. There was scant evidence for character release: insular mustelines do not evolve towards the size of a missing guild member, nor is sexual size dimorphism greater on islands. There was no evidence for a lower limit on the size similarity of co-existing mustelids.
Main conclusions  We propose that different guild compositions in different localities produce different evolutionary trajectories. Similar sizes on islands and mainlands can be explained by similar prey sizes in both settings. Morphological evidence suggests that competition is probably not a ubiquitous force in the assembly and evolution of musteline guilds.     

An intraspecific comparative analysis of character divergence between sympatric species

Although sympatric character divergence between closely related species has been described in a wide variety of taxa, the evolutionary processes responsible for generating these patterns are difficult to identify. One hypothesis that can explain sympatric differences is ecological character displacement: the sympatric origin of morphologically divergent phenotypes in response to selection caused by interspecific competition. Alternatively, populations may adapt to different conditions in allopatry, with sympatric distributions evolving through selective colonization and proliferation of ecologically compatible phenotypes. In this study, I characterize geographic variation within two sibling species of rocky-shore gastropods that have partially overlapping distributions in central California. In sympatry, both Nucella emarginata and N. ostrina show significant differences in shell shape and shell ornamentation that together suggest that where the two species co-exist, divergent phenotypes arose as an evolutionary consequence of competition. To examine the evolutionary origins of divergent characters in sympatry, I used a comparative method based on spatial autocorrelation to remove the portion of the phenotypic variance among populations that is explained by genetic distance (using mitochondrial DNA sequences and allozyme frequency data). Because the remaining portion of the phenotypic variance represents the independent divergence of individual populations, a significant sympatric difference in the corrected dataset provides evidence of true character displacement: significant sympatric character evolution that is independent of population history. After removal of genetic distance effects in Nucella, shell shape differences remain statistically significant in N. emarginata, providing evidence of significant sympatric character divergence. However, for external shell ornamentation in both species and shell shape in N. ostrina, the significance of sympatric differences is lost in the corrected dataset, indicating that colonization events and gene flow have played important roles in the evolutionary history of character divergence in sympatry. Although the absence of a widely dispersing planktonic larva in the life cycle of Nucella will promote local adaptation, the results here indicate that once advantageous traits arise, demographic processes, such as recurrent gene flow between established populations and extinction and recolonization, are important factors contributing to the geographic pattern of sympatric character divergence.     

Community-wide character displacement in the presence of clines: a test of Holarctic weasel guilds

1. Competition is thought to be a major influence on community assembly, ecology and evolution; presence of competitors may cause divergence in traits related to resource use (character displacement). 2. Such traits, however, often vary clinally, and this phenomenon may be independent of the presence or absence of competing species. 3. The presence of such clines can either obscure the effects of competition, or create an impression that competition is operating when, in fact, it is not. 4. We corrected for clinal variation while testing for character displacement in two well-studied weasel (Mustela) guilds, in the Nearctic and the west Palaearctic. 5. Without accounting for clines, our results agreed with previous studies suggesting character displacement in these guilds. 6. However, when we corrected for clines, predictions of competition theory were not met - and often we obtained evidence for character convergence in sympatry. 7. This may suggest that the nature of the resource base may be more important than interspecific competition in shaping morphology and size in these carnivores. 8. Our results highlight the need to account for geographic variation when studying character displacement and cast some doubt on prevailing ideas regarding the effect of competition on morphological evolution.     

The role of interspecific interference competition in character displacement and the evolution of competitor recognition

The extent to which interspecific interference competition has contributed to character evolution is one of the most neglected problems in evolutionary biology. When formerly allopatric species come into secondary contact, aggressive interactions between the species can cause selection on traits that affect interspecific encounter rates (e.g. habitat preferences, activity schedules), competitor recognition (e.g. colouration, song), and fighting ability (e.g. weaponry, body size). We define agonistic character displacement (ACD) as the process of phenotypic evolution in a population caused by interference competition with one or more sympatric species and which results in shifts in traits that affect the rate, intensity or outcome of interspecific aggression. After clarifying the relationships between ACD and other evolutionary processes that may occur when species come into secondary contact, we develop an individual‐based, quantitative genetic model to examine how traits involved in competitor recognition would be expected to evolve under different secondary contact scenarios. Our simulation results show that both divergence and convergence are possible outcomes, depending on the intensity of interspecific exploitative competition, the costs associated with mutual versus unilateral recognition, and the extent of phenotypic differences prior to secondary contact. We then devise a set of eight criteria for evaluating putative examples of ACD and review the empirical literature to assess the strength of existing evidence and to identify promising avenues for future research. Our literature search revealed 33 putative examples of ACD across insects, fishes, bats, birds, lizards, and amphibians (15 divergence examples; 18 convergence examples). Only one example satisfies all eight criteria for demonstrating ACD, but most case studies satisfy four or more criteria. The current state of the evidence for ACD is similar to the state of the evidence for ecological character displacement just 10 years ago. We conclude by offering suggestions for further theoretical and empirical research on ACD.     

ECOLOGICAL ORIGIN OF MORPHOLOGICAL DIVERSITY: A STUDY OF ALTERNATIVE TROPHIC PHENOTYPES IN LARVAL SALAMANDERS

The role of ecological factors in promoting morphological diversity within and among species is an area of debate among evolutionary biologists. Using morphological differences between sympatric species as evidence that competition promotes divergence (e.g., character displacement), has, in particular, drawn harsh criticism because morphological differences may have evolved during allopatry. In contrast to species, alternative phenotypes within a species have a common phylogenetic history, so differences between phenotypes are likely to result from ecological conditions experienced in sympatry. Using cannibal and typical larval phenotypes of the Arizona tiger salamander, Ambystoma tigrinum nebulosum, we tested two predictions of the hypothesis that resource competition promotes morphological divergence: (1) larval phenotypes should reduce competition by using different resources; and (2) the advantage to developing the alternative, cannibal phenotype should be highest when competition among typical larvae is most intense. We used field surveys and a field experiment to test these predictions. The two larval phenotypes used different resources, especially when competition was intense. The advantage to individual larvae of becoming cannibals was highest when competition for resources among typical larvae was high. These results support the hypothesis that resource competition can promote morphological divergence.     

Community-wide character displacement in Miocene hyaenas

Recent studies have found regularities in the pattern of distribution of dental parameters such as canine or carnassial length among sympatric carnivores. These regularities are taken to be indicative of community-wide character displacement. This study documents similar patterns in late Miocene and earliest Pliocene hyaenids from several localities in Eurasia and Africa. Statistical tests show ratios of lower carnassial total lengths and blade lengths between species to be suggestively equal among sympatric late Miocene hyaenas. Other measurements do not show this regular pattern. This finding mirrors that regarding modern canids in the Middle East, suggesting that a process leading to community-wide character displacement was in effect among these hyaenid taxa. Their response to this pattern suggests that they occupied a similar ecological role to modern canids. The causal basis for such a process is unknown but is suggested to lie in direct interspecific competition between carnivores rather than being a response to regularly spaced features of the environment. Character displacement, competition, Hyaenidae, Miocene, Eurasia, Africa.     

Allelopathic adaptation can cause competitive coexistence

The maintenance of plant diversity is often explained by the ecological and evolutionary consequences of resource competition. Recently, the importance of allelopathy for competitive interactions has been recognized. In spite of such interest in allelopathy, we have few theories for understanding how the allelopathy influences the ecological and evolutionary dynamics of competing species. Here, I study the coevolutionary dynamics of two competing species with allelopathy in an interspecific competition system, and show that adaptive trait dynamics can cause cyclic coexistence. In addition, very fast adaptation such as phenotypic plasticity is likely to stabilize the population cycles. The results suggest that adaptive changes in allelopathy can lead to cyclic coexistence of plant species even when their ecological characters are very similar and interspecific competition is stronger than intraspecific competition, which should destroy competitive coexistence in the absence of adaptation.     

How does the magnitude of genetic variation affect ecological and reproductive character displacement?

While previous studies on character displacement tended to focus on trait divergence and convergence as a result of long-term evolution, recent studies suggest that character displacement can be a special case of evolutionary rescue, where rapid evolution prevents species extinction by weakening interspecific competition. Here we analyzed a simple model to examine how the magnitude of genetic variation affects evolutionary rescue via ecological and reproductive character displacement that weakens interspecific competition in exploitation of shared resources (i.e., resource competition) and in the mating process caused by incomplete species recognition (i.e., reproductive interference), respectively. We found that slow trait divergence due to small genetic variance results in species extinction in reproductive character displacement but not in ecological character displacement. This is because one species becomes rare in slow character displacement, and this causes deterministic extinction due to minority disadvantage of reproductive interference. On the other hand, there is no deterministic extinction in the process of ecological character displacement. Furthermore, species extinction becomes less likely in the case of positive covariance between ecological and reproductive traits as divergence of the ecological trait (e.g., root depths) increases the divergence speed of the reproductive trait (e.g., flower colors) and vice versa. It will be interesting to compare intraspecific genetic (co)variance of ecological and reproductive traits in future studies for understanding how ecological and reproductive character displacement occur without extinction.     

Spatial patterns,ecological niches,and interspecific competition of avian brood parasites: inferring from a case study of Korea

Since obligate avian brood parasites depend completely on the effort of other host species for rearing their progeny, the availability of hosts will be a critical resource for their life history. Circumstantial evidence suggests that intense competition for host species may exist not only within but also between species. So far, however, few studies have demonstrated whether the interspecific competition really occurs in the system of avian brood parasitism and how the nature of brood parasitism is related to their niche evolution. Using the occurrence data of five avian brood parasites from two sources of nationwide bird surveys in South Korea and publically available environmental/climatic data, we identified their distribution patterns and ecological niches, and applied species distribution modeling to infer the effect of interspecific competition on their spatial distribution. We found that the distribution patterns of five avian brood parasites could be characterized by altitude and climatic conditions, but overall their spatial ranges and ecological niches extensively overlapped with each other. We also found that the predicted distribution areas of each species were generally comparable to the realized distribution areas, and the numbers of individuals in areas where multiple species were predicted to coexist showed positive relationships among species. In conclusion, despite following different coevolutionary trajectories to adapt to their respect host species, five species of avian brood parasites breeding in South Korea occupied broadly similar ecological niches, implying that they tend to conserve ancestral preferences for ecological conditions. Furthermore, our results indicated that contrary to expectation interspecific competition for host availability between avian brood parasites seemed to be trivial, and thus, play little role in shaping their spatial distributions and ecological niches. Future studies, including the complete ranges of avian brood parasites and ecological niches of host species, will be worthwhile to further elucidate these issues.     

The genome as a life-history character: why rate of molecular evolution varies between mammal species

DNA sequences evolve at different rates in different species. This rate variation has been most closely examined in mammals, revealing a large number of characteristics that can shape the rate of molecular evolution. Many of these traits are part of the mammalian life-history continuum: species with small body size, rapid generation turnover, high fecundity and short lifespans tend to have faster rates of molecular evolution. In addition, rate of molecular evolution in mammals might be influenced by behaviour (such as mating system), ecological factors (such as range restriction) and evolutionary history (such as diversification rate). I discuss the evidence for these patterns of rate variation, and the possible explanations of these correlations. I also consider the impact of these systematic patterns of rate variation on the reliability of the molecular date estimates that have been used to suggest a Cretaceous radiation of modern mammals, before the final extinction of the dinosaurs.     

Experimental evidence that competition between stickleback species favours adaptive character divergence

The ecological character displacement hypothesis assumes that the effects of interspecific resource competition cause divergent selection to favour phenotypes that exploit non-shared resources. This model predicts that interspecific competition declines with increased divergence. Direct tests of this decline are rare despite much comparative evidence for character displacement. We tested this prediction using a pair of divergent brook sticklebacks. Brook sticklebacks sympatric with ninespine sticklebacks have diverged from local allopatric brook populations, and so the two types of brook sticklebacks potentially represent pre- and post-displacement forms. We used enclosures placed in a lake to compare short-term fitness (growth) of sympatric (post-displacement) and allopatric (pre-displacement) brook forms in the presence and absence of ninespine sticklebacks. Brook sticklebacks grew less in the presence vs. absence of ninespine sticklebacks, indicating that interspecific competition occurred. As expected, allopatric brook forms had lower growth than sympatric forms when ninespine sticklebacks were present. This result suggests that ecological character displacement has occurred.     

Inferring speciation modes in a clade of Iberian chafers from rates of morphological evolution in different character systems

Background  

Studies of speciation mode based on phylogenies usually test the predicted effect on diversification patterns or on geographical distribution of closely related species. Here we outline an approach to infer the prevalent speciation mode in Iberian Hymenoplia chafers through the comparison of the evolutionary rates of morphological character systems likely to be related to sexual or ecological selection. Assuming that mitochondrial evolution is neutral and not related to measured phenotypic differences among the species, we contrast hypothetic outcomes of three speciation modes: 1) geographic isolation with subsequent random morphological divergence, resulting in overall change proportional to the mtDNA rate; 2) sexual selection on size and shape of the male intromittent organs, resulting in an evolutionary rate decoupled to that of the mtDNA; and 3) ecological segregation, reflected in character systems presumably related to ecological or biological adaptations, with rates decoupled from that of the mtDNA.     

Testing the role of interspecific competition in the evolutionary origin of elevational zonation: an example with Buarremon brush-finches (Aves, Emberizidae) in the neotropical mountains

Interspecific competition might drive the evolution of ecological niches and result in pairs of formerly competing species segregating along ecological gradients following a process of character displacement. This mechanism has been proposed to account for replacement of related species along gradients of elevation in many areas of the world, but the fundamental issue of whether competition is responsible for the origin of elevational replacements has not been tested. To test hypotheses about the role of interspecific competition in the origin of complementary elevational ranges, I combined molecular phylogenetics, phylogeography, and population genetic analyses on Buarremon torquatus and B. brunneinucha (Aves, Emberizidae), whose patterns of elevational distribution suggest character displacement or ecological release. The hypothesis that elevational distributions in these species changed in opposite directions as a result of competition is untenable because: (1) a historical expansion of the range of B. brunneinucha into areas occupied by B. torquatus was not accompanied by a shift in the elevational range of the former species; (2) when B. brunneinucha colonized the range of B. torquatus, lineages of the latter distributions had already diverged; and (3) historical trends in effective population size do not suggest populations with elevational ranges abutting those of putative competitors have declined as would be expected if competition caused range contractions. However, owing to uncertainty in coalescent estimates of historical population sizes, the hypothesis that some populations of B. torquatus have declined cannot be confidently rejected, which suggests asymmetric character displacement might have occurred. I suggest that the main role of competition in elevational zonation may be to act as a sorting mechanism that allows the coexistence along mountain slopes only of ecologically similar species that differ in elevational distributions prior to attaining sympatry. The contrasting biogeographic histories of B. brunneinucha and B. torquatus illustrate how present-day ecological interactions can have recent origins, and highlights important challenges for testing the hypothesis of character displacement in the absence of data on population history and robust reconstructions of the evolution of traits and geographic ranges.     

Reproductive interference between animal species

Although sexual interactions between species (reproductive interference) have been reported from a wide range of animal taxa, their potential for determining species coexistence is often disregarded. Here, we review evidence from laboratory and field studies illustrating that heterospecific sexual interactions are frequently associated with fitness loss and can have severe ecological and evolutionary consequences. We define reproductive interference as any kind of interspecific interaction during the process of mate acquisition that adversely affects the fitness of at least one of the species involved and that is caused by incomplete species recognition. We distinguish seven types of reproductive interference: signal jamming, heterospecific rivalry, misdirected courtship, heterospecific mating attempts, erroneous female choice, heterospecific mating, and hybridization. We then discuss the sex-specific costs of these types and highlight two typical features of reproductive interference: density-dependence and asymmetry. Similar to competition, reproductive interference can lead to displacement of one species (sexual exclusion), spatial, temporal, or habitat segregation, changes in life history parameters, and reproductive character displacement. In many cases, patterns of coexistence might be shaped by reproductive interference rather than by resource competition, as the presence of a few heterospecifics might substantially decrease reproductive success. Therefore, interspecific sexual interactions should receive more attention in ecological research. Reproductive interference has mainly been discussed in the context of invasive species or hybrid zones, whereas its influence on naturally-occurring sympatric species pairs has rarely been addressed. To improve our knowledge of the ecological significance of reproductive interference, findings from laboratory experiments should be validated in the field. Future studies should also focus on ecological mechanisms, such as temporal spatial, or habitat partitioning, that might enable sexually interacting species to coexist. Reproductive interference also has implications for the management of endangered species, which can be threatened by sexual interactions with invasive or common species. Studies of reproductive interference might even provide new insights for biological pest control.