Sex,competition and mimicry: an eco-evolutionary model reveals unexpected impacts of ecological interactions on the evolution of phenotypes in sympatry

Phenotypic evolution in sympatric species can be strongly impacted by species interactions, either mutualistic or antagonistic. Heterospecific reproductive behaviours between sympatric species have been shown to favour phenotypic divergence of traits used as sexual cues. Those traits may also be involved in local adaptation or in other types of species interactions and, as a result, undergo complex evolutions across sympatric species. Here we focus on mimicry and study how reproductive interference may impair phenotypic convergence between species with various levels of defence. We use a deterministic model assuming two sympatric species where individuals can display two different warning colour patterns. This eco-evolutionary model explores how ecological interactions shape phenotypic evolution within sympatric species. We investigate the effect of 1) the opposing density-dependent selections exerted on colour patterns by predation and reproductive behaviour and 2) the impact of relative species and phenotype abundances on the fitness costs faced by each individual depending on their species and phenotype. Our model shows that reproductive interference may limit the convergent effect of mimetic interactions and may promote phenotypic divergence between Müllerian mimics. The divergent and convergent evolution of traits also strongly depends on the relative species and phenotype abundances and levels of trophic competition, highlighting how the eco-evolutionary feedbacks between phenotypic evolution and species abundances may result in strikingly different evolutionary routes.     

Independent contrasts succeed where ancestor reconstruction fails in a known bacteriophage phylogeny

Abstract.— Methods of ancestor reconstruction are important tools for evolutionary inference that are difficult to test empirically because ancestral states are rarely known with certainty. We evaluated reconstruction methods for continuous phenotypic characters using taxa from an experimentally generated bacteriophage phylogeny. Except for one slowly evolving character, the estimated ancestral states of continuous phenotypic characters were highly inaccurate and biased, even when including a known ancestor at the root. This error was caused by a directional trend in character evolution and by rapid rates of character evolution. Computer simulations confirmed that such factors affect reconstruction of continuous characters in general. We also used phenotypic viral characters to evaluate two methods that attempt to estimate the correlation between characters during evolution. Whereas a nonphylogenetic regression was relatively inaccurate and biased, independent contrasts accurately estimated the correlation between characters with little bias.     

Criticality Is an Emergent Property of Genetic Networks that Exhibit Evolvability

Accumulating experimental evidence suggests that the gene regulatory networks of living organisms operate in the critical phase, namely, at the transition between ordered and chaotic dynamics. Such critical dynamics of the network permits the coexistence of robustness and flexibility which are necessary to ensure homeostatic stability (of a given phenotype) while allowing for switching between multiple phenotypes (network states) as occurs in development and in response to environmental change. However, the mechanisms through which genetic networks evolve such critical behavior have remained elusive. Here we present an evolutionary model in which criticality naturally emerges from the need to balance between the two essential components of evolvability: phenotype conservation and phenotype innovation under mutations. We simulated the Darwinian evolution of random Boolean networks that mutate gene regulatory interactions and grow by gene duplication. The mutating networks were subjected to selection for networks that both (i) preserve all the already acquired phenotypes (dynamical attractor states) and (ii) generate new ones. Our results show that this interplay between extending the phenotypic landscape (innovation) while conserving the existing phenotypes (conservation) suffices to cause the evolution of all the networks in a population towards criticality. Furthermore, the networks produced by this evolutionary process exhibit structures with hubs (global regulators) similar to the observed topology of real gene regulatory networks. Thus, dynamical criticality and certain elementary topological properties of gene regulatory networks can emerge as a byproduct of the evolvability of the phenotypic landscape.     

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.     

Phenotypic similarity and differentiation among sympatric cryptic species in a freshwater amphipod species complex

1. Cryptic species diversity poses evolutionary questions about its origin and maintenance, and ecological questions about the coexistence of seemingly identical species. 2. We examine patterns of morphological and life history differentiation in three sympatric cryptic species of freshwater amphipods within the Hyalella azteca species complex. These species are separated by extensive molecular evolution, but appear similar in phenotype. Species were collected from the littoral zone of a small kettle lake in Michigan, U.S.A., and identified to species by molecular genetic methods. 3. Two of the species were similar, differing only in female size, whereas the third was larger in body size and had larger clutches of smaller eggs than the other two. There were differences between the species also in pleon spine length and antennal segment number. 4. An analysis of allozyme variation among the cryptic species in three lakes suggests that the species are reproductively isolated within lakes. 5. We suggest that phenotypic similarity of these species is maintained by size‐selective predation by fish. The small, but statistically significant, differences in body size may form the axis for a tradeoff between resource exploitation and predator avoidance, a condition that can foster coexistence of phenotypically similar species.     

Adaptive diversification of a plastic trait in a predictably fluctuating environment

There is substantial evidence that evolutionary diversification can occur in allopatric conditions through reduction in the degree of phenotypic plasticity when an isolated population encounters a novel, more stable environment. Plasticity is no longer favored in the new environment, either because it carries an inherent physiological cost or because it leads to production of suboptimal phenotypes. In order to explore the role of phenotypic plasticity in sympatric diversification, we modeled the ecological and evolutionary dynamics of Escherichia coli bacteria in batch cultures. Our results describe an evolutionary pathway leading to metabolic diversification in a sympatric environment without spatial structure. In an environment that fluctuates widely and predictably, evolutionary branching leads to diversification and stable coexistence of generalist and specialist ecotypes for some combinations of parameters. Diversification and stable coexistence occur when reaction norms are steep and trade-offs between metabolic pathways are convex. We conclude that, in principle, diversification due to reduced plasticity can occur without allopatric isolation, reduced environmental variability, or an explicit cost of plasticity.     

CAN PARALLEL DIVERSIFICATION OCCUR IN SYMPATRY? REPEATED PATTERNS OF BODY‐SIZE EVOLUTION IN COEXISTING CLADES OF NORTH AMERICAN SALAMANDERS

A classic paradigm in evolutionary biology is that geographically isolated clades inhabiting similar selective regimes will diversify to create similar sets of phenotypes in different locations (e.g., similar stickleback species in different lakes, similar Anolis ecomorphs on different islands). Such parallel radiations are not generally expected to occur in sympatry because the available niche space would be filled by whichever clade is diversified first. Here, we document a very different pattern, the parallel evolution of similar body-size morphs in three sympatric clades of plethodontid salamanders ( Desmognathus, Plethodon, Spelerpinae) in eastern North America. Using a comprehensive, time-calibrated phylogeny of North American plethodontids from nuclear and mitochondrial DNA sequences, we show that these three clades have undergone replicated patterns of evolution in body size and that this parallel diversification occurred in broad-scale sympatry. At the local scale, we find that coexisting species from these clades are more similar in body size than expected under a null model in which species are randomly assembled into communities. These patterns are particularly surprising in that competition is known to be important in driving phenotypic diversification and limiting local coexistence of similar-sized species within these clades. Although parallel diversification of sympatric clades may seem counterintuitive, we discuss several ecological and evolutionary factors that may allow the phenomenon to occur.     

Mechanical reproductive isolation via divergent genital morphology between Carabus insulicola and C. esakii with implications in species coexistence

The mechanical isolation hypothesis predicts that physical incompatibility between divergent reproductive morphologies hinders hybridization between populations. However, evidence for this hypothesis remains scarce. We examined this hypothesis using two parapatric carabid beetles, Carabus insulicola and C. esakii, which are of the subgenus Ohomopterus and exhibit a species-specific genital lock-and-key system. Our interspecific crossing experiment revealed that incompatibility of genital morphologies served as a strong postmating-prezygotic isolation barrier. This isolation was asymmetric: a decrease in female fitness was more costly in the cross with greater genitalic incompatibility between a C. esakii female and a C. insulicola male. These two species share a limited sympatric area, but the mechanism responsible for their coexistence is unclear given no evidence of premating isolation via male mate choice. A comparison of the present results with those of previous studies that quantified reproductive isolation between Ohomopterus species suggest that strong mechanical isolation via genitalic incompatibility plays a major role in species isolation, but that it may be less important in species coexistence.     

Phenotypic plasticity of mate recognition systems prevents sexual interference between two sympatric leaf beetle species

Maladaptive sexual interactions among heterospecific individuals (sexual interference) can prevent the coexistence of animal species. Thus, the avoidance of sexual interference by divergence of mate recognition systems is crucial for a stable coexistence in sympatry. Mate recognition systems are thought to be under tight genetic control. However, we demonstrate that mate recognition systems of two closely related sympatric leaf beetle species show a high level of host‐induced phenotypic plasticity. Mate choice in the mustard leaf beetles, Phaedon cochleariae and P. armoraciae, is mediated by cuticular hydrocarbons (CHCs). Divergent host plant use causes a divergence of CHC phenotypes, whereas similar host use leads to their convergence. Consequently, both species exhibit significant behavioral isolation when they feed on alternative host species, but mate randomly when using a common host. Thus, sexual interference between these syntopic leaf beetles is prevented by host‐induced phenotypic plasticity rather than by genotypic divergence of mate recognition systems.     

Novelty and emergent patterns in sperm: Morphological diversity and evolution of spermatozoa and sperm conjugation in ground beetles (Coleoptera: Carabidae)

The beetle family Carabidae, with about 40,000 species, exhibits enough diversity in sperm structure and behavior to be an excellent model system for studying patterns and processes of evolution. We explore their potential, documenting sperm form in 177 species of ground beetles using light microscopy and collecting data on one qualitative and seven quantitative phenotypic traits. Our sampling captures 61% of the tribal-level diversity of ground beetles. These data highlight the notable morphological diversity of sperm in ground beetles and suggest that sperm in the group have dynamic evolutionary histories with much morphological innovation and convergence. Sperm vary among species in total length (48–3,400 μm), head length (0.5–270 μm), and head width (0.2–6.3 μm). Most ground beetles make sperm with heads that are indistinct from the flagella at the gross morphological level. However, some or all Omophron, Trachypachus, and Dyschiriini make broad-headed sperm that show morphological differences between species. Most ground beetles package their sperm into groups of sperm, termed conjugates, and ground beetles show variation in conjugate form and in the number and arrangement of sperm in a conjugate. Most ground beetles make sperm conjugates by embedding their sperm in a hyaline rod or spermatostyle. The spermatostyle is remarkably variable among species and varies in length from 17 to 41,000 μm. Several unrelated groups of ground beetles make only singleton sperm, including Nebriinae, Cicindelinae, many Trechinae, and the tribe Paussini. In order to study patterns in sperm evolution, we combine these data with a low-resolution phylogeny of ground beetles. Results from modern comparative analyses suggest the following: (a) sperm differ from conjugates in some aspect of their underlying evolutionary process, (b) sperm have influenced conjugate evolution and vice versa, and (c) conjugation with a spermatostyle likely evolved early within the history of Carabidae and it has been lost independently at least three times.     

Evolution of early embryogenesis in rhabditid nematodes

The cell-biological events that guide early-embryonic development occur with great precision within species but can be quite diverse across species. How these cellular processes evolve and which molecular components underlie evolutionary changes is poorly understood. To begin to address these questions, we systematically investigated early embryogenesis, from the one- to the four-cell embryo, in 34 nematode species related to C. elegans. We found 40 cell-biological characters that captured the phenotypic differences between these species. By tracing the evolutionary changes on a molecular phylogeny, we found that these characters evolved multiple times and independently of one another. Strikingly, all these phenotypes are mimicked by single-gene RNAi experiments in C. elegans. We use these comparisons to hypothesize the molecular mechanisms underlying the evolutionary changes. For example, we predict that a cell polarity module was altered during the evolution of the Protorhabditis group and show that PAR-1, a kinase localized asymmetrically in C. elegans early embryos, is symmetrically localized in the one-cell stage of Protorhabditis group species. Our genome-wide approach identifies candidate molecules—and thereby modules—associated with evolutionary changes in cell-biological phenotypes.     

Sexual selection at the protein level drives the extraordinary divergence of sex-related genes during sympatric speciation

An increasing number of molecular studies are indicating that, in a wide variety of species, genes directly related to fertilization evolve at extraordinarily high rates. We try to gain insight into the dynamics of this rapid evolution and its underlying mechanisms by means of a simple theoretical model. In the model, sexual selection and sympatric speciation act together in order to drive rapid divergence of gamete recognition proteins. In this process, intraspecific competition for fertilizations enlarges male gamete protein variation by means of evolutionary branching, which initiates sympatric speciation. In addition, avoidance of competition for fertilizations between the incipient species drives the rapid evolution of gamete recognition proteins. This mechanism can account for both strong stabilizing selection on gamete recognition proteins within species and rapid divergence between species. Moreover, it can explain the empirical finding that the rate of divergence of fertilization genes is not constant, but highest between closely related species.     

Quantifying Reproductive Barriers in a Sympatric Pair of Darter Species

Quantifying and comparing the strengths of different reproductive barriers between diverging lineages is especially useful for determining the evolutionary mechanisms driving speciation. Etheostoma barrenense and Etheostoma zonale are closely related sympatric species of darters that are sexually dimorphic and exhibit clear differences in male nuptial coloration. Prior studies demonstrated that these species exhibit complete behavioral isolation, and that both intraspecific and interspecific variation in male coloration play a role in female choice, all consistent with speciation by sexual selection on male nuptial color. Remaining unclear, however, is whether behavioral isolation is the strongest reproductive barrier between these species or, alternatively, whether additional reproductive barriers are equally strong, which could implicate mechanisms other than sexual selection in speciation. Here, we compare the relative strengths of multiple reproductive barriers between the two focal species, measuring: (1) ecological isolation, (2) gametic incompatibility, (3) hybrid inviability, (4) conspecific sperm precedence, and comparing these measures to a previously estimated strength of behavioral isolation. We find that behavioral isolation is the strongest reproductive barrier measured to date and suggest it may be the only barrier that has evolved to completion. This result provides additional empirical evidence for speciation driven by sexual selection and provides insight into the maintenance of sympatric species in nature.     

Labile male morphology and intraspecific male polymorphism in the Philotrypesis fig wasps

We investigate the evolution of male morphology in the fig wasps belonging to the genus Philotrypesis (Chalcidoidea, Sycorectinae). We first reconstruct the phylogenetic relationships of Philotrypesis associated with African figs using nuclear and mitochondrial DNA. We then determine male morphotypes in the species included in our phylogeny and show that intraspecific polymorphism is common. Most species present two types of males and some species have up to three types. These morphotypes are believed to represent alternative mating tactics: some males show morphological adaptations to fighting, others are winged dispersers and others are small sneakers. Mapping out these variations onto our phylogeny reveals that the combination of morphs changes randomly along the branches of the tree. Both parsimony and likelihood approaches indicate that there has been at least one transition from dimorphism to trimorphism, several gains and losses of the small morph and two independent acquisitions of the winged morph. Using maximum likelihood analyses of character evolution, we estimate transition rates for each morph and show that the evolution of each type of morph are not correlated and that forward and backward transition rates are not significantly different. Our results altogether suggest that male morphology is evolutionary labile, it responds quickly to selection imposed by the mating environment. This study, also suggests that seemingly complex phenotypes, such as winged males, can evolve several times and can even be recreated after having been lost.     

Diversification on an ecologically constrained adaptive landscape

We used phylogenetic analysis of body-size ecomorphs in a crustacean species complex to gain insight into how spatial complexity of ecological processes generates and maintains biological diversity. Studies of geographically widespread species of Hyalella amphipods show that phenotypic evolution is tightly constrained in a manner consistent with adaptive responses to alternative predation regimes. A molecular phylogeny indicates that evolution of Hyalella ecomorphs is characterized by parallel evolution and by phenotypic stasis despite substantial levels of underlying molecular change. The phylogeny suggests that species diversification sometimes occurs by niche shifts, and sometimes occurs without a change in niche. Moreover, diversification in the Hyalella ecomorphs has involved the repeated evolution of similar phenotypic forms that exist in similar ecological settings, a hallmark of adaptive evolution. The evolutionary stasis observed in clades separated by substantial genetic divergence, but existing in similar habitats, is also suggestive of stabilizing natural selection acting to constrain phenotypic evolution within narrow bounds. We interpret the observed decoupling of genetic and phenotypic diversification in terms of adaptive radiation on an ecologically constrained adaptive landscape, and suggest that ecological constraints, perhaps acting together with genetic and functional constraints, may explain the parallel evolution and evolutionary stasis inferred by the phylogeny.     

The evolution of coexistence: Reciprocal adaptation promotes the assembly of a simple community

Species coexistence may result by chance when co‐occurring species do not strongly interact or it may be an evolutionary outcome of strongly interacting species adapting to each other. Although patterns like character displacement indicate that coexistence has often been an evolutionary outcome, it is unclear how often the evolution of coexistence represents adaptation in only one species or reciprocal adaptation among all interacting species. Here, we demonstrate a strong role for evolution in the coexistence of guppies and killifish in Trinidadian streams. We experimentally recreated the temporal stages in the invasion and establishment of guppies into communities that previously contained only killifish. We combined demographic responses of guppies and killifish with a size‐based integral projection model to calculate the fitness of the phenotypes of each species in each of the stages of community assembly. We show that guppies from locally adapted populations that are sympatric with killifish have higher fitness when paired with killifish than guppies from allopatric populations. This elevated fitness involves effects traceable to both guppy and killifish evolution. We discuss the implications of our results to the study of species coexistence and how it may be mediated through eco‐evolutionary feedbacks.     

INTERSEXUAL ARMS RACE? GENITAL COEVOLUTION IN NEPHILID SPIDERS (ARANEAE,NEPHILIDAE)

Genital morphology is informative phylogenetically and strongly selected sexually. We use a recent species-level phylogeny of nephilid spiders to synthesize phylogenetic patterns in nephilid genital evolution that document generalized conflict between male and female interests. Specifically, we test the intersexual coevolution hypothesis by defining gender-specific indices of genital complexity that summarize all relevant and phylogenetically informative traits. We then use independent contrasts to show that male and female genital complexity indices correlate significantly and positively across the phylogeny rather than among sympatric sister species, as predicted by reproductive character displacement. In effect, as females respond to selection for fecundity-driven fitness via giantism and polyandry (perhaps responding to male-biased effective sex ratios), male mechanisms evolve to monopolize females (male monogamy) via opportunistic mating, pre- and postcopulatory mate guarding, and/or plugging of female genitalia to exclude subsequent suitors. In males morphological symptoms of these phenomena range from self-mutilated genitalia to total castration. Although the results are compatible with both recently favored sexual selection hypotheses, sexually antagonistic coevolution, and cryptic female choice, the evidence of strong intersexual conflict and genitalic damage in both sexes is more easily explained as sexually antagonistic coevolution due to an evolutionary arms race.     

Testing whether ecological factors promote cladogenesis in a group of tiger beetles (Coleoptera: Cicindelidae)

We investigate the role of ecological differentiation in cladogenesis of a monophyletic group of North American tiger beetles, the subgenus Ellipsoptera (genus: Cicindela), by reconstructing their species-level phylogeny from mitochondrial DNA sequences. Observed reconstructions of ecological characters on the phylogeny are compared to those expected under simple null models of no association with cladogenesis. We find no evidence that ecological disparity is associated with either species coexistence, speciation or long-term persistence and/or radiation of lineages. Ecomorphological traits have evolved in response to differences in habitat occupied by species, but without detectable relationship with cladogenesis.     

Experimental Removal of Sexual Selection Reveals Adaptations to Polyandry in Both Sexes

Polyandrous mating is extremely common, yet for many species the evolutionary significance is not fully resolved. In order to understand the evolution of mating systems, it is crucial that we investigate the adaptive consequences across many facets of reproduction. We performed experimental evolution with the naturally polygamous flour beetle Tribolium castaneum subjected to either polyandry or enforced monogamy, creating contrasting selection regimes associated with the presence or absence of sexual selection. After 36 generations, we investigated male and female adaptations by mating beetles with an unselected tester strain to exclude potential effects of male–female coevolution. Reproductive success of focal monogamous and polyandrous beetles from each sex was assessed in separate single male and multiple male experiments emulating the different selection backgrounds. Males and females from the polyandrous regime had more offspring in the experiments with multiple males present than monogamous counterparts. However, in single male experiments, neither females nor males differed between selection regimes. Subsequent mating trials with multiple males suggested that adaptations to polyandry in both sexes provide benefits when choice and competition were allowed to take place. Polyandrous females delayed the first copulation when given a choice of males and polyandrous males were quicker to achieve copulation when facing competition. In conclusion, we show that the expected benefits of evolutionary adaptation to polyandry in T. castaneum depended on the availability of multiple mates. This context-dependent effect, which concerned both sexes, highlights the importance of realistic competition and choice experiments.     

Large Spatial Scale of the Phenotype-Environment Color Matching in Two Cryptic Species of African Desert Jerboas (Dipodidae: Jaculus)

We tested the camouflage hypothesis, or the linkage between animal (Saharan rodent) and habitat coloration, on the largest geographical scale yet conducted. We aimed to determine whether phenotypic variation is explained by micro-habitat variation and/or genetic polymorphism to determine 1) the strength of linkage between fur color and local substrate color, and 2) the divergence in fur coloration between two genetic clades, representing cryptic species, throughout the complete range of the African desert jerboas (Jaculus jaculus). We used a combination of museum and field-collected specimens, remote sensing tools, satellite and digital photography and molecular genetic and phylogenetic methods to investigate the above hypotheses. Along with showing that the two divergent genetic clades of jerboas occur sympatrically throughout their African distribution, we showed significant covariation between dorsal fur coloration of the animals and the color of their habitat. We also described significant phenotypic divergence in fur color, consistent with genetic divergence between the sympatric clades. The linkage between environment and phenotype supports the idea that the selection promoting cryptic coloration is persistent in contemporary populations of jerboas, however the phenotypic divergence indicates that it has different strengths (or optima) in the two clades. The mosaic distribution of micro-habitats occupied by geographically sympatric clades suggests that it may influence both ecological and evolutionary dynamics between these two cryptic species.