Testing hypotheses about ecological specialization using phylogenetic trees

It is often assumed that ecological specialization represents an evolutionary "dead-end" that limits further evolution. Maximum-likelihood (ML) analyses on phylogenies for 15 groups of phytophagous insects revealed that high transition rates both to and from specialization occurred, but that the mean ratio of rates was significantly biased toward a higher rate to specialization. Here we explore the consequences of the fact that transition rates inferred by ML are affected not only by the distribution, but also by the frequency, of character states. Higher rates to the more common state were inferred in the analyses of Nosil (2002), in similar studies published since 2002, and in a small set of simulations. Thus, the ratio of the rate toward versus away from specialization was strongly, positively correlated with the proportion of specialist species at the tips of the phylogeny and whether transitions away from specialization occur remains unclear. Here we reexamine these data using methods that do not rely on directly comparing transition rates. Maximum-likelihood analyses show that models with no transitions in one direction (e.g., irreversible evolution as predicted by the "specialist as dead end" framework) are usually strongly rejected, independent of the proportion of specialists at the tips. Ancestral state reconstruction revealed two instances where generalists were unambiguously derived from specialists. Transition rates would need to biased 100-fold and 5000-fold toward specialization to reconstruct a history where these shifts from specialization toward generalization do not occur. The general conclusions of Nosil (2002) appear to hold; transitions in either direction likely occur such that specialization does not always limit further evolution. Most generally, inferences regarding character evolution can be strengthened by comparing models of character change and examining ancestor states, rather than only comparing parameter values.     

ABRUPT DECELERATION OF MOLECULAR EVOLUTION LINKED TO THE ORIGIN OF ARBORESCENCE IN FERNS

Molecular rate heterogeneity, whereby rates of molecular evolution vary among groups of organisms, is a well‐documented phenomenon. Nonetheless, its causes are poorly understood. For animals, generation time is frequently cited because longer‐lived species tend to have slower rates of molecular evolution than their shorter‐lived counterparts. Although a similar pattern has been uncovered in flowering plants, using proxies such as growth form, the underlying process has remained elusive. Here, we find a deceleration of molecular evolutionary rate to be coupled with the origin of arborescence in ferns. Phylogenetic branch lengths within the “tree fern” clade are considerably shorter than those of closely related lineages, and our analyses demonstrate that this is due to a significant difference in molecular evolutionary rate. Reconstructions reveal that an abrupt rate deceleration coincided with the evolution of the long‐lived tree‐like habit at the base of the tree fern clade. This suggests that a generation time effect may well be ubiquitous across the green tree of life, and that the search for a responsible mechanism must focus on characteristics shared by all vascular plants. Discriminating among the possibilities will require contributions from various biological disciplines, but will be necessary for a full appreciation of molecular evolution.     

Is specialization an evolutionary dead end? Testing for differences in speciation,extinction and trait transition rates across diverse phylogenies of specialists and generalists

Specialization has often been claimed to be an evolutionary dead end, with specialist lineages having a reduced capacity to persist or diversify. In a phylogenetic comparative framework, an evolutionary dead end may be detectable from the phylogenetic distribution of specialists, if specialists rarely give rise to large, diverse clades. Previous phylogenetic studies of the influence of specialization on macroevolutionary processes have demonstrated a range of patterns, including examples where specialists have both higher and lower diversification rates than generalists, as well as examples where the rates of evolutionary transitions from generalists to specialists are higher, lower or equal to transitions from specialists to generalists. Here, we wish to ask whether these varied answers are due to the differences in macroevolutionary processes in different clades, or partly due to differences in methodology. We analysed ten phylogenies containing multiple independent origins of specialization and quantified the phylogenetic distribution of specialists by applying a common set of metrics to all datasets. We compared the tip branch lengths of specialists to generalists, the size of specialist clades arising from each evolutionary origin of a specialized trait and whether specialists tend to be clustered or scattered on phylogenies. For each of these measures, we compared the observed values to expectations under null models of trait evolution and expected outcomes under alternative macroevolutionary scenarios. We found that specialization is sometimes an evolutionary dead end: in two of the ten case studies (pollinator‐specific plants and host‐specific flies), specialization is associated with a reduced rate of diversification or trait persistence. However, in the majority of studies, we could not distinguish the observed phylogenetic distribution of specialists from null models in which specialization has no effect on diversification or trait persistence.     

Loss of sexual recombination and segregation is associated with increased diversification in evening primroses

The loss of sexual recombination and segregation in asexual organisms has been portrayed as an irreversible process that commits asexually reproducing lineages to reduced diversification. We test this hypothesis by estimating rates of speciation, extinction, and transition between sexuality and functional asexuality in the evening primroses. Specifically, we estimate these rates using the recently developed BiSSE (Binary State Speciation and Extinction) phylogenetic comparative method, which employs maximum likelihood and Bayesian techniques. We infer that net diversification rates (speciation minus extinction) in functionally asexual evening primrose lineages are roughly eight times faster than diversification rates in sexual lineages, largely due to higher speciation rates in asexual lineages. We further reject the hypothesis that a loss of recombination and segregation is irreversible because the transition rate from functional asexuality to sexuality is significantly greater than zero and in fact exceeded the reverse rate. These results provide the first empirical evidence in support of the alternative theoretical prediction that asexual populations should instead diversify more rapidly than sexual populations because they are free from the homogenizing effects of sexual recombination and segregation. Although asexual reproduction may often constrain adaptive evolution, our results show that the loss of recombination and segregation need not be an evolutionary dead end in terms of diversification of lineages.     

Rate heterogeneity, ancestral character state reconstruction, and the evolution of limb morphology in Lerista (Scincidae, Squamata)

Rates of phenotypic evolution derive from numerous interrelated processes acting at varying spatial and temporal scales and frequently differ substantially among lineages. Although current models employed in reconstructing ancestral character states permit independent rates for distinct types of transition (forward and reverse transitions and transitions between different states), these rates are typically assumed to be identical for all branches in a phylogeny. In this paper, I present a general model of character evolution enabling rate heterogeneity among branches. This model is employed in assessing the extent to which the assumption of uniform transition rates affects reconstructions of ancestral limb morphology in the scincid lizard clade Lerista and, accordingly, the potential for rate variability to mislead inferences of evolutionary patterns. Permitting rate variation among branches significantly improves model fit for both the manus and the pes. A constrained model in which the rate of digit acquisition is assumed to be effectively zero is strongly supported in each case; when compared with a model assuming unconstrained transition rates, this model provides a substantially better fit for the manus and a nearly identical fit for the pes. Ancestral states reconstructed assuming the constrained model imply patterns of limb evolution differing significantly from those implied by reconstructions for uniform-rate models, particularly for the pes; whereas ancestral states for the uniform-rate models consistently entail the reacquisition of pedal digits, those for the model incorporating among-lineage rate heterogeneity imply repeated, unreversed digit loss. These results indicate that the assumption of identical transition rates for all branches in a phylogeny may be inappropriate in modeling the evolution of phenotypic traits and emphasize the need for careful evaluation of phylogenetic tests of Dollo's law.     

Exploring among-site rate variation models in a maximum likelihood framework using empirical data: effects of model assumptions on estimates of topology,branch lengths,and bootstrap support

We have investigated the effects of different among-site rate variation models on the estimation of substitution model parameters, branch lengths, topology, and bootstrap proportions under minimum evolution (ME) and maximum likelihood (ML). Specifically, we examined equal rates, invariable sites, gamma-distributed rates, and site-specific rates (SSR) models, using mitochondrial DNA sequence data from three protein-coding genes and one tRNA gene from species of the New Zealand cicada genus Maoricicada. Estimates of topology were relatively insensitive to the substitution model used; however, estimates of bootstrap support, branch lengths, and R-matrices (underlying relative substitution rate matrix) were strongly influenced by the assumptions of the substitution model. We identified one situation where ME and ML tree building became inaccurate when implemented with an inappropriate among-site rate variation model. Despite the fact the SSR models often have a better fit to the data than do invariable sites and gamma rates models, SSR models have some serious weaknesses. First, SSR rate parameters are not comparable across data sets, unlike the proportion of invariable sites or the alpha shape parameter of the gamma distribution. Second, the extreme among-site rate variation within codon positions is problematic for SSR models, which explicitly assume rate homogeneity within each rate class. Third, the SSR models appear to give severe underestimates of R-matrices and branch lengths relative to invariable sites and gamma rates models in this example. We recommend performing phylogenetic analyses under a range of substitution models to test the effects of model assumptions not only on estimates of topology but also on estimates of branch length and nodal support.     

Life history affects the evolution of reproductive isolation among species of Coreopsis (Asteraceae)

The evolution of reproductive isolation within Coreopsis is investigated by integrating phylogenetic data with estimates of pollen viability of plants from inter- and intraspecific crosses. Three different models that predict F1 fitness are compared. The first uses ITS pairwise distances, the second is based on phylogenetic branch lengths derived from DNA sequences, and the third elaborates on the second model by dividing branch length according to reconstructions of the evolution of life history. This is the first study to use phylogenetic branch-length estimates for predicting levels of reproductive isolation. Estimated branch lengths (model 2) predict hybrid fitness more accurately than simply genetic distance (model 1) but only very slightly. This is probably because the two variables are strongly correlated in Coreopsis. Prediction is substantially improved by allowing evolutionary rates to differ between annual and perennial branches (model 3). A bootstrapping procedure indicates that the life-history effect is statistically significant. The more rapid evolution of reproductive isolation within annual species of Coreopsis may be due to differing mechanisms of reproductive isolation, that is, chromosomal rearrangements rather than genetic incompatibilities.     

Standardized phylogenetic tree: a reference to discover functional evolution

Functional evolution is often driven by positive natural selection. Although it is thought to be rare in evolution at the molecular level, its effects may be observed as the accelerated evolutionary rates. Therefore one of the effective ways to identify functional evolution is to identify accelerated evolution. Many methods have been developed to test the statistical significance of the accelerated evolutionary rate by comparison with the appropriate reference rate. The rates of synonymous substitution are one of the most useful and popular references, especially for large-scale analyses. On the other hand, these rates are applicable only to a limited evolutionary time period because they saturate quickly--i.e., multiple substitutions happen frequently because of the lower functional constraint. The relative rate test is an alternative method. This technique has an advantage in terms of the saturation effect but is not sufficiently powerful when the evolutionary rate differs considerably among phylogenetic lineages. For the aim to provide a universal reference tree, we propose a method to construct a standardized tree which serves as the reference for accelerated evolutionary rate. The method is based upon multiple molecular phylogenies of single genes with the aim of providing higher reliability. The tree has averaged and normalized branch lengths with standard deviations for statistical neutrality limits. The standard deviation also suggests the reliability level of the branch order. The resulting tree serves as a reference tree for the reliability level of the branch order and the test of evolutionary rate acceleration even when some of the species lineages show an accelerated evolutionary rate for most of their genes due to bottlenecking and other effects.     

Comparison of site-specific rate-inference methods for protein sequences: empirical Bayesian methods are superior

The degree to which an amino acid site is free to vary is strongly dependent on its structural and functional importance. An amino acid that plays an essential role is unlikely to change over evolutionary time. Hence, the evolutionary rate at an amino acid site is indicative of how conserved this site is and, in turn, allows evaluation of its importance in maintaining the structure/function of the protein. When using probabilistic methods for site-specific rate inference, few alternatives are possible. In this study we use simulations to compare the maximum-likelihood and Bayesian paradigms. We study the dependence of inference accuracy on such parameters as number of sequences, branch lengths, the shape of the rate distribution, and sequence length. We also study the possibility of simultaneously estimating branch lengths and site-specific rates. Our results show that a Bayesian approach is superior to maximum-likelihood under a wide range of conditions, indicating that the prior that is incorporated into the Bayesian computation significantly improves performance. We show that when branch lengths are unknown, it is better first to estimate branch lengths and then to estimate site-specific rates. This procedure was found to be superior to estimating both the branch lengths and site-specific rates simultaneously. Finally, we illustrate the difference between maximum-likelihood and Bayesian methods when analyzing site-conservation for the apoptosis regulator protein Bcl-x(L).     

RECURRENT EVOLUTION OF DIOECY IN BRYOPHYTES

The origin and maintenance of separate sexes (dioecy) is an enduring evolutionary puzzle. Although both hermaphroditism and dioecy occur in many diverse clades, we know little about the long‐term evolutionary consequences of changing sexual system. Here we find evidence for at least 133 transitions between sexual systems in mosses, representing an almost unparalleled lability in the evolution of their sexual systems. Furthermore, in contrast to predictions, the transition rate from hermaphroditism to dioecy was approximately twice as high as the reverse transition. Our results also suggest that hermaphrodites may have higher rates of diversification than dioecious mosses. These results illustrate the utility of mosses for understanding the genomic and macroevolutionary consequences of hermaphroditism and dioecy.     

Ecological and Ecomorphological Specialization Are Not Associated with Diversification Rates in Muroid Rodents (Rodentia: Muroidea)

Multiple diversification rate shifts explain uneven clade richness in muroid rodents. Previous muroid studies have shown that extrinsic factors, notwithstanding ecological opportunity, are poor predictors of clade diversity. Here, we use a 297-muroid species chronogram that is sampled proportional to total clade diversity, along with various trait-dependent diversification approaches to investigate the association between diversification rates with intrinsic attributes—diet, habitat, body mass, and relative tail length. We found some association between both dietary specialization and body mass, as well as between habitat specialization with relative tail lengths using phylogenetic analyses of variance. However, there was no significant association between diversification rates with the evolution of these traits in muroid rodents. We also show that several of the state-dependent diversification approaches are highly susceptible to Type I error—a result that is in accordance with recent criticisms of these methods. Finally, we discuss several potential causes for the lack of association between the examined trait data with diversification rates, ranging from methodological biases (e.g. method conservativism) to biology (e.g. behavioral plasticity and ecological opportunism of muroid rodents).     

Trophic network structure emerges through antagonistic coevolution in temporally varying environments

Understanding the mechanisms underlying ecological specialization is central to our understanding of community ecology and evolution. Although theoretical work has investigated how variable environments may affect specialization in single species, little is known about how such variation impacts bipartite network structure in antagonistically coevolving systems. Here, we develop and analyse a general model of victim-enemy coevolution that explicitly includes resource and population dynamics. We investigate how temporal environmental heterogeneity affects the evolution of specialization and associated community structure. Environmental productivity influences victim investment in resistance, which will shape patterns of specialization through its regulating effect on enemy investment in infectivity. We also investigate the epidemiological consequences of environmental variability and show that enemy population density is maximized for intermediate lengths of productive seasons, which corresponds to situations where enemies can evolve higher infectivity than victims can evolve defence. We discuss our results in the light of empirical studies, and further highlight ways in which our model applies to a range of natural systems.     

Body size effects and rates of cytochrome b evolution in tube-nosed seabirds

Variation in rates of molecular evolution now appears to be widespread. The demonstration that body size is correlated with rates of molecular evolution suggests that physiological and ecological factors may be involved in molecular rate variation, but large-scale comparative studies are still lacking. Here, we use complete cytochrome b sequences from 85 species of tube-nosed seabirds (order Procellariiformes) and 5 outgroup species of penguins (order Sphenisciformes) to test for an association between body mass and rates of molecular evolution within the former avian order. Cladistic analysis of the 90 sequences estimates a phylogeny largely consistent with the traditional taxonomy of the Procellariiformes. The Diomedeidae, Procellariidae, and Pelecanoididae are monophyletic, while the Hydrobatidae are basal and paraphyletic. However, the two subfamilies within the Hydrobatidae (Hydrobatinae and Oceanitinae) are monophyletic. A likelihood ratio test detects significant deviation from clocklike evolution in our data. Using a sign test for an association between body mass and branch length in the seabird phylogeny, we find that larger taxa tend to have shorter terminal branch lengths than smaller taxa. This observation suggests that rates of mitochondrial DNA evolution are slower for larger taxa. Rate calibrations based on the fossil record reveal concordant body size effects. We interpret these results as evidence for a metabolic rate effect, as the species in this order exhibit large differences in metabolic rates, which are known to be highly correlated with body mass in this group. Our results support previous findings of body size effects and show that this effect can be significant even within a single avian order. This suggests that even lineage-specific molecular clocks may not be tenable if calibrations involve taxa with different metabolic rates.      

Trophic specialization influences the rate of environmental niche evolution in damselfishes (Pomacentridae)

The rate of environmental niche evolution describes the capability of species to explore the available environmental space and is known to vary among species owing to lineage-specific factors. Trophic specialization is a main force driving species evolution and is responsible for classical examples of adaptive radiations in fishes. We investigate the effect of trophic specialization on the rate of environmental niche evolution in the damselfish, Pomacentridae, which is an important family of tropical reef fishes. First, phylogenetic niche conservatism is not detected in the family using a standard test of phylogenetic signal, and we demonstrate that the environmental niches of damselfishes that differ in trophic specialization are not equivalent while they still overlap at their mean values. Second, we estimate the relative rates of niche evolution on the phylogenetic tree and show the heterogeneity among rates of environmental niche evolution of the three trophic groups. We suggest that behavioural characteristics related to trophic specialization can constrain the evolution of the environmental niche and lead to conserved niches in specialist lineages. Our results show the extent of influence of several traits on the evolution of the environmental niche and shed new light on the evolution of damselfishes, which is a key lineage in current efforts to conserve biodiversity in coral reefs.     

Neutral theory, phylogenies, and the relationship between phenotypic change and evolutionary rates

The neutral theory of molecular evolution predicts that rates of phenotypic change are largely independent from genotypic change. A recent study by Bromham et al. (2002) confirmed this expectation, finding no evidence for correlated phenotypic and molecular evolutionary rates in animals. We reevaluate this hypothesis, sampling at different taxonomic levels in plants and animals, using Bayesian inference to reconstruct phylogenetic trees and estimate rates of molecular evolution. We use independent contrasts in branch lengths to maximize the information extracted from each of the trees and nodal posterior probabilities to assess the influence of phylogenetic error. Our results indicate that in vascular plants between 2% and 11% of the variation in phenotypic rates of change can be explained by the rate of genotypic change. These results may be explained by the idea that processes that affect general evolutionary rates, such as body size, may also be expected to influence rates of morphological change.     

Effects of branch length errors on the performance of phylogenetically independent contrasts

We examined Type I error rates of Felsenstein's (1985; Am. Nat. 125:1-15) comparative method of phylogenetically independent contrasts when branch lengths are in error and the model of evolution is not Brownian motion. We used seven evolutionary models, six of which depart strongly from Brownian motion, to simulate the evolution of two continuously valued characters along two different phylogenies (15 and 49 species). First, we examined the performance of independent contrasts when branch lengths are distorted systematically, for example, by taking the square root of each branch segment. These distortions often caused inflated Type I error rates, but performance was almost always restored when branch length transformations were used. Next, we investigated effects of random errors in branch lengths. After the data were simulated, we added errors to the branch lengths and then used the altered phylogenies to estimate character correlations. Errors in the branches could be of two types: fixed, where branch lengths are either shortened or lengthened by a fixed fraction; or variable, where the error is a normal variate with mean zero and the variance is scaled to the length of the branch (so that expected error relative to branch length is constant for the whole tree). Thus, the error added is unrelated to the microevolutionary model. Without branch length checks and transformations, independent contrasts tended to yield extremely inflated and highly variable Type I error rates. Type I error rates were reduced, however, when branch lengths were checked and transformed as proposed by Garland et al. (1992; Syst. Biol. 41:18-32), and almost never exceeded twice the nominal P-value at alpha = 0.05. Our results also indicate that, if branch length transformations are applied, then the appropriate degrees of freedom for testing the significance of a correlation coefficient should, in general, be reduced to account for estimation of the best branch length transformation. These results extend those reported in Díaz-Uriarte and Garland (1996; Syst. Biol. 45:27-47), and show that, even with errors in branch lengths and evolutionary models different from Brownian motion, independent contrasts are a robust method for testing hypotheses of correlated evolution.     

Inferring complex DNA substitution processes on phylogenies using uniformization and data augmentation

A new method is developed for calculating sequence substitution probabilities using Markov chain Monte Carlo (MCMC) methods. The basic strategy is to use uniformization to transform the original continuous time Markov process into a Poisson substitution process and a discrete Markov chain of state transitions. An efficient MCMC algorithm for evaluating substitution probabilities by this approach using a continuous gamma distribution to model site-specific rates is outlined. The method is applied to the problem of inferring branch lengths and site-specific rates from nucleotide sequences under a general time-reversible (GTR) model and a computer program BYPASSR is developed. Simulations are used to examine the performance of the new program relative to an existing program BASEML that uses a discrete approximation for the gamma distributed prior on site-specific rates. It is found that BASEML and BYPASSR are in close agreement when inferring branch lengths, regardless of the number of rate categories used, but that BASEML tends to underestimate high site-specific substitution rates, and to overestimate intermediate rates, when fewer than 50 rate categories are used. Rate estimates obtained using BASEML agree more closely with those of BYPASSR as the number of rate categories increases. Analyses of the posterior distributions of site-specific rates from BYPASSR suggest that a large number of taxa are needed to obtain precise estimates of site-specific rates, especially when rates are very high or very low. The method is applied to analyze 45 sequences of the alpha 2B adrenergic receptor gene (A2AB) from a sample of eutherian taxa. In general, the pattern expected for regions under negative selection is observed with third codon positions having the highest inferred rates, followed by first codon positions and with second codon positions having the lowest inferred rates. Several sites show exceptionally high substitution rates at second codon positions that may represent the effects of positive selection.     

The information content of a character under a Markov model of evolution

The rate of evolutionary change associated with a character determines its utility for the reconstruction of phylogenetic history. For a given age of lineage splits, we examine the information content of a character to assess the magnitude and range of an optimal rate of substitution. On the one hand an optimal transition rate must provide sufficiently many character changes to distinguish subclades, whereas on the other hand changes must be sufficiently rare that reversals on a single branch (and hence homoplasy) are uncommon. In this study, we evolve binary characters over three tree topologies with fixed branch lengths, while varying transition rate as a parameter. We use the character state distribution obtained to measure the "information content" of a character given a transition rate. This is done with respect to several criteria-the probability of obtaining the correct tree using parsimony, the probability of infering the correct ancestral state, and Shannon-Weaver and Fisher information measures on the configuration of probability distributions. All of the information measures suggest the intuitive result of the existence of optimal rates for phylogeny reconstruction. This nonzero optimum is less pronounced if one conditions on there having been a change, in which case the parsimony-based results of minimum change being the most informative tends to hold.     

DNA evolutionary rates in nine-primaried passerine birds

Differences in single-copy nuclear-DNA sequences among 13 species of passerine birds were measured using DNA-DNA hybridization. A matrix of pairwise dissimilarity values (delta mode distances) was constructed from analysis of fitted thermal dissociation curves. A least-squares method of phylogenetic estimation was used to construct two topologies from the distance matrix, one constraining branch lengths of sister taxa to be equal and the other permitting such lengths to vary. These topologies were identical in the pattern of branching of taxa, and the difference in their sums of squares was not statistically significant, suggesting that rates of DNA evolution in sister groups of nine- primaried oscines are equal. A nonparametric test for nonrandom variation in distances of sister groups to outgroup taxa revealed no statistically significant deviation from random variation that would be expected as a result of measurement error. However, the level of measurement error was such that rates of DNA evolution in sister taxa could vary by as much as 10% without being detected with the statistical methods used here.      

Phenotypic plasticity and specialization in clonal versus non-clonal plants: A data synthesis

Reproductive strategies can be associated with ecological specialization and generalization. Clonal plants produce lineages adapted to the maternal habitat that can lead to specialization. However, clonal plants frequently display high phenotypic plasticity (e.g. clonal foraging for resources), factors linked to ecological generalization. Alternately, sexual reproduction can be associated with generalization via increasing genetic variation or specialization through rapid adaptive evolution. Moreover, specializing to high or low quality habitats can determine how phenotypic plasticity is expressed in plants. The specialization hypothesis predicts that specialization to good environments results in high performance trait plasticity and specialization to bad environments results in low performance trait plasticity. The interplay between reproductive strategies, phenotypic plasticity, and ecological specialization is important for understanding how plants adapt to variable environments. However, we currently have a poor understanding of these relationships. In this study, we addressed following questions: 1) Is there a relationship between phenotypic plasticity, specialization, and reproductive strategies in plants? 2) Do good habitat specialists express greater performance trait plasticity than bad habitat specialists? We searched the literature for studies examining plasticity for performance traits and functional traits in clonal and non-clonal plant species from different habitat types. We found that non-clonal (obligate sexual) plants expressed greater performance trait plasticity and functional trait plasticity than clonal plants. That is, non-clonal plants exhibited a specialist strategy where they perform well only in a limited range of habitats. Clonal plants expressed less performance loss across habitats and a more generalist strategy. In addition, specialization to good habitats did not result in greater performance trait plasticity. This result was contrary to the predictions of the specialization hypothesis. Overall, reproductive strategies are associated with ecological specialization or generalization through phenotypic plasticity. While specialization is common in plant populations, the evolution of specialization does not control the nature of phenotypic plasticity as predicted under the specialization hypothesis.