Exploring the Macroevolutionary Signature of Asymmetric Inheritance at Speciation.

Popular comparative phylogenetic models such as Brownian Motion, Ornstein-Ulhenbeck, and their extensions, assume that, at speciation, a trait value is inherited identically by two descendant species. This assumption contrasts with models of speciation at a micro-evolutionary scale where descendants' phenotypic distributions are sub-samples of the ancestral distribution. Different speciation mechanisms can lead to a displacement of the ancestral phenotypic mean among descendants and an asymmetric inheritance of the ancestral phenotypic variance. In contrast, even macro-evolutionary models that account for intraspecific variance assume symmetrically conserved inheritance of ancestral phenotypic distribution at speciation. Here we develop an Asymmetric Brownian Motion model (ABM) that relaxes the assumption of symmetric and conserved inheritance of the ancestral distribution at the time of speciation. The ABM jointly models the evolution of both intra- and inter-specific phenotypic variation. It also infers the mode of phenotypic inheritance at speciation, which can range from a symmetric and conserved inheritance, where descendants inherit the ancestral distribution, to an asymmetric and displaced inheritance, where descendants inherit divergent phenotypic means and variances. To demonstrate this model, we analyze the evolution of beak morphology in Darwin finches, finding evidence of displacement at speciation. The ABM model helps to bridge micro- and macro-evolutionary models of trait evolution by providing a more robust framework for testing the effects of ecological speciation, character displacement, and niche partitioning on trait evolution at the macro-evolutionary scale.

Mechanisms of coexistence: Exploring species sorting and character displacement in woody plants to alleviate belowground competition.

Rarely do we observe competitive exclusion within plant communities, even though plants compete for a limited pool of resources. Thus, our understanding of the mechanisms sustaining plant biodiversity might be limited. In this study, we explore two common ecological strategies, species sorting and character displacement, that promote coexistence by reducing competition. We assess the degree to which woody plants may implement these two strategies to lower belowground competition for nutrients which occurs via nutritional (mostly mycorrhizal) mutualisms. First, we compile data on plant traits and the mycorrhizal association state of woody angiosperms using a global inventory of indigenous flora. Our analysis reveals that species in locations with high mycorrhizal diversity exhibit distinct mean values in leaf area and wood density based on their mycorrhizal type, indicating species sorting. Second, we reanalyse a large dataset on leaf area to demonstrate that in areas with high mycorrhizal diversity, trees maintain divergent leaf area values, showcasing character displacement. Character displacement among plants is considered rare, making our observation significant. In summary, our study uncovers a rare occurrence of character displacement and identifies a common mechanism employed by plants to alleviate competition, shedding light on the complexities of plant coexistence in diverse ecosystems.

Competitive Displacement and Agonistic Character Displacement, or the Ghost of Interference Competition.

AbstractInterference competition can drive species apart in habitat use through competitive displacement in ecological time and agonistic character displacement (ACD) over evolutionary time. As predicted by ACD theory, sympatric species of rubyspot damselflies (Hetaerina spp.) that respond more aggressively to each other in staged encounters differ more in microhabitat use. However, the same pattern could arise from competitive displacement if dominant species actively exclude subordinate species from preferred microhabitats. The degree to which habitat partitioning is caused by competitive displacement can be assessed with removal experiments. We carried out removal experiments with three species pairs of rubyspot damselflies. With competitive displacement, removing dominant species should allow subordinate species to shift into the dominant species' microhabitat. Instead, we found that species-specific microhabitat use persisted after the experimental removals. Thus, the previously documented association between heterospecific aggression and microhabitat partitioning in this genus is most likely a product of divergence in habitat preferences caused by interference competition in the evolutionary past.

The role of divergent host use and geography in the evolution of habitat isolation and sexual isolation among sister species of Belonocnema gall wasps.

Ecology and geography can play important roles in the evolution of reproductive isolation across the speciation continuum, but few studies address both at the later stages of speciation. This notable gap in knowledge arises from the fact that traditional ecological speciation studies have predominantly focused on the role of ecology in initiating the speciation process, while many studies exploring the effect of geography (e.g., reinforcement) concentrate on species pairs that lack divergent ecological characteristics. We simultaneously examine the strength of habitat isolation and sexual isolation among three closely related species of Belonocnema gall-forming wasps on two species of live oaks, Quercus virginiana and Q. geminata, that experience divergent selection from their host plants and variable rates of migration due to their geographic context. We find that the strength of both habitat isolation and sexual isolation is lowest among allopatric species pairs with the same host plant association, followed by allopatric species with different host plant associations, and highest between sympatric species with different host-plant associations. This pattern suggests that divergent selection due to different host use interacts with geography in the evolution of habitat isolation and sexual isolation during the later stages of speciation of Belonocnema wasps.

Variations in water economy traits in two Sphagnum species across their distribution boundaries.

PREMISE: We assessed changes in traits associated with water economy across climatic gradients in the ecologically similar peat mosses Sphagnum cuspidatum and Sphagnum lindbergii. These species have parapatric distributions in Europe and have similar niches in bogs. Sphagnum species of bogs are closely related, with a large degree of microhabitat niche overlap between many species that can be functionally very similar. Despite this, ecologically similar species do have different distributional ranges along climatic gradients that partly overlap. These gradients may favor particular Sphagnum traits, especially in relation to water economy, which can be hypothesized to drive species divergence by character displacement. METHODS: We investigated traits relevant for water economy of two parapatric bryophytes (Sphagnum cuspidatum and S. lindbergii) across the border of their distributional limits. We included both shoot traits and canopy traits, i.e., collective traits of the moss surface, quantified by photogrammetry. RESULTS: The two species are ecologically similar and occur at similar positions along the hydrological gradient in bogs. The biggest differences between the species were expressed in the variations of their canopy surfaces, particularly surface roughness and in the responses of important traits such as capitulum mass to climate. We did not find support for character displacement, because traits were not more dissimilar in sympatric than in allopatric populations. CONCLUSIONS: Our results suggest that parapatry within Sphagnum can be understood from just a few climatic variables and that climatic factors are stronger drivers than competition behind trait variation within these species of Sphagnum.

Character displacement drives trait divergence in a continental fauna.

Coexisting (sympatric) pairs of closely related species are often characterized by exaggerated trait differences. This widespread pattern is consistent with adaptation for reduced similarity due to costly interactions (i.e., "character displacement")-a classic hypothesis in evolutionary theory. But it is equally consistent with a community assembly bias in which lineages with greater trait differences are more likely to establish overlapping ranges in the first place (i.e., "species sorting"), as well as with null expectations of trait divergence through time. Few comparative analyses have explicitly modeled these alternatives, and it remains unclear whether trait divergence is a general prerequisite for sympatry or a consequence of interactions between sympatric species. Here, we develop statistical models that allow us to distinguish the signature of these processes based on patterns of trait divergence in closely related lineage pairs. We compare support for each model using a dataset of bill shape differences in 207 pairs of New World terrestrial birds representing 30 avian families. We find that character displacement models are overwhelmingly supported over species sorting and null expectations, indicating that exaggerated bill shape differences in sympatric pairs result from enhanced divergent selection in sympatry. We additionally detect a latitudinal gradient in character displacement, which appears strongest in the tropics. Our analysis implicates costly species interactions as powerful drivers of trait divergence in a major vertebrate fauna. These results help substantiate a long-standing but equivocally supported linchpin of evolutionary theory.

Species divergence under competition and shared predation.

Species competing for resources also commonly share predators. While competition often drives divergence between species, the effects of shared predation are less understood. Theoretically, competing prey species could either diverge or evolve in the same direction under shared predation depending on the strength and symmetry of their interactions. We took an empirical approach to this question, comparing antipredator and trophic phenotypes between sympatric and allopatric populations of threespine stickleback and prickly sculpin fish that all live in the presence of a trout predator. We found divergence in antipredator traits between the species: in sympatry, antipredator adaptations were relatively increased in stickleback but decreased in sculpin. Shifts in feeding morphology, diet and habitat use were also divergent but driven primarily by stickleback evolution. Our results suggest that asymmetric ecological character displacement indirectly made stickleback more and sculpin less vulnerable to shared predation, driving divergence of antipredator traits between sympatric species.

Rapid evolution of ecological sexual dimorphism driven by resource competition.

Sex differences in ecologically important traits are common in animals and plants, and prompted Darwin to first propose an ecological cause of sexual dimorphism. Despite theoretical plausibility and Darwin's original notion, a role for ecological resource competition in the evolution of sexual dimorphism has never been directly demonstrated and remains controversial. I used experimental evolution in Drosophila melanogaster to test the hypothesis that resource competition can drive the evolution of sex differences in diet. Following just three generations of adaptation, offspring from flies evolved in low-resource, high-competition environments show elevated sexual dimorphism in diet preference compared to both the ancestor and populations evolved on high-resource availability. This increased sexual dimorphism was the result of divergence in male sucrose intake and female yeast intake consistent with the differential nutritional requirements of the sexes. These results provide the first real-time direct evidence for evolution of sexual dimorphism driven by resource competition.

Ecological and evolutionary consequences of selective interspecific information use.

Recent work has shown that animals frequently use social information from individuals of their own species as well as from other species; however, the ecological and evolutionary consequences of this social information use remain poorly understood. Additionally, information users may be selective in their social information use, deciding from whom and how to use information, but this has been overlooked in an interspecific context. In particular, the intentional decision to reject a behaviour observed via social information has received less attention, although recent work has indicated its presence in various taxa. Based on existing literature, we explore in which circumstances selective interspecific information use may lead to different ecological and coevolutionary outcomes between two species, such as explaining observed co-occurrences of putative competitors. The initial ecological differences and the balance between the costs of competition and the benefits of social information use potentially determine whether selection may lead to trait divergence, convergence or coevolutionary arms race between two species. We propose that selective social information use, including adoption and rejection of behaviours, may have far-reaching fitness consequences, potentially leading to community-level eco-evolutionary outcomes. We argue that these consequences of selective interspecific information use may be much more widespread than has thus far been considered.

Reproductive isolation via divergent genital morphology due to cascade reinforcement in Ohomopterus ground beetles.

Secondary contact between incipient species and selection against maladaptive hybridization can drive reinforcement between populations in contact and result in reproductive character displacement (RCD). Resultant divergence in mating traits within a species may generate downstream reproductive isolation between populations with displaced and non-displaced traits, referred to as the cascade reinforcement hypothesis. We examined this hypothesis using three allopatric populations of the ground beetle Carabus maiyasanus with a genital lock-and-key system. This species shows RCD in male and female genital morphologies in populations in contact with the sister species C. iwawakianus. In a reciprocal mating experiment using three allopatric populations with differences in male and female genital sizes, insemination failure increased as the difference in genital size increased. Based on the reproductive isolation index, insemination failure was the major postmating-prezygotic isolation barrier, at least in one population pair with comparable total isolation to those of other species pairs. By contrast, there was only incomplete premating isolation among populations. These results suggest that RCD in genital morphologies drives incipient allopatric speciation, supporting the cascade reinforcement hypothesis. These findings provide insight into the roles of interspecific interactions and subsequent trait diversification in speciation processes.

Males and females contribute differently to the evolution of habitat segregation driven by hybridization.

Costly heterospecific mating interactions, such as hybridization, select for prezygotic reproductive isolation. One of the potential traits responding to the selection arising from maladaptive hybridization is habitat preference, whose divergence results in interspecific habitat segregation. Theoretical studies have so far assumed that habitat preference is a sexually shared trait. However, male and female habitat preferences can experience different selection pressures. Here, by combining analytical and simulation approaches, we theoretically examine the evolution of sex-specific habitat preferences. Habitat segregation can have demographic consequences, potentially generating eco-evolutionary dynamics. We thus explicitly consider demography in the simulation model. We also vary the degrees of species discrimination to examine how mate choice influences the evolution of habitat preferences. Results show that both sexes can reduce hybridisation risk by settling in the habitats where abundant conspecific mates reside. However, when females can discriminate species, excess conspecific male aggregation intensifies male-male competition for mating opportunities, posing an obstacle to conspecific aggregation. Meanwhile, conspecific female aggregation attracts conspecific males, by offering the mating opportunity. Therefore, under effective species discrimination, females play a leading role in initiating habitat use divergence. Simulations typically result in either the coexistence with established habitat segregation or the extinction of one of the species. The former result is especially likely when the species differ to some extent in habitat preferences upon secondary contact. Our results disentangle the selection pressures acting on male and female habitat preferences, deepening our understanding of the evolutionary process of habitat segregation due to hybridization.

Evolution of ontogenetic niches promotes species coexistence in a surprising way.

Animals usually change their trophic niche during their ontogeny, which has fundamental consequences for their population dynamics and interactions with other species. Theory predicts that ontogenetic niche differences between species can influence their ability to coexist. However, we lack empirical evidence for this coexistence mechanism and the role of evolution in shaping species' ontogenetic niches. Here, Anaya-Rojas et al. (2023) show that contemporary evolution of ontogenetic niches likely contributes to the coexistence of two competing fish species (killifish and guppies) in streams on the Caribbean Island of Trinidad. As predicted by coexistence theory, they found that the weaker competitor (killifish) exhibited a relatively large ontogenetic niche shift, feeding at higher trophic levels as it grew, in streams where competition with the stronger competitor (guppies) was intense. Intuition suggests that the weaker competitor should experience strong selection on its ontogenetic niche in a different competitive environment, but this was not the case. Instead, they found that the stronger competitor evolved a more compressed ontogenetic niche, where guppies fed at a low trophic level regardless of their body size, when competition was intense. Although the mechanism underlying this surprising result remains to be determined, this work points to the importance of taking a food web perspective-explicitly accounting for consumer-resource interactions-to understand the outcome of eco-evolutionary dynamics. Given that ontogenetic niche shifts are extremely common in animals, understanding the evolutionary ecology of these niche shifts should be a priority for future research on species coexistence.

Incomplete partitioning of pollinators by Linum suffruticosum and its coflowering congeners.

PREMISE: Linum suffruticosum shows variations in pollinator fit, pollen pickup, and local pollinators that predict pollen deposition rates. The species often coflowers with other Linum species using the same pollinators. We investigated whether L. suffruticosum trait variation could be explained by local patterns of pollinator sharing and associated evolution to reduce interspecific pollen transfer. METHODS: Pollinator observations were made in different localities (single species, coflowering with other congeners). Floral traits were measured to detect differences across populations and from coflowering species. Reproductive costs were quantified using interspecific hand pollinations and measures of pollen-tube formation, combined with observations of pollen arrival on stigmas and pollen-tube formation after natural pollination in allopatric and sympatric localities. RESULTS: The size and identity of the most important pollinator of L. suffruticosum and whether there was pollinator sharing with coflowering species appeared to explain floral trait variation related to pollinator fit. The morphological overlap of the flowers of L. suffruticosum with those of coflowering species varied, depending on coflowering species identity. A post-pollination incompatibility system maintains reproductive isolation, but conspecific pollen-tube formation was lower after heterospecific pollination. Under natural pollination at sites of coflowering with congeners, conspecific pollen-tube formation was lower than at single-species localities. CONCLUSIONS: Trait variation in L. suffruticosum appears to respond to the most important local pollinator. Locally, incomplete pollinator partitioning might cause interspecific pollination, imposing reproductive costs. These reproductive costs may generate selection on floral traits for reduced morphological overlap with coflowering congeners, leading to the evolution of pollination ecotypes.

The latitudinal gradient in rates of evolution for bird beaks, a species interaction trait.

Where is evolution fastest? The biotic interactions hypothesis proposes that greater species richness creates more ecological opportunity, driving faster evolution at low latitudes, whereas the 'empty niches' hypothesis proposes that ecological opportunity is greater where diversity is low, spurring faster evolution at high latitudes. We tested these contrasting predictions by analysing rates of beak evolution for a global dataset of 1141 avian sister species. Rates of beak size evolution are similar across latitudes, with some evidence that beak shape evolves faster in the temperate zone, consistent with the empty niches hypothesis. The empty niches hypothesis is further supported by a meta-analysis showing that rates of trait evolution and recent speciation are generally faster in the temperate zone, whereas rates of molecular evolution are slightly faster in the tropics. Our results suggest that drivers of evolutionary diversification are either similar across latitudes or more potent in the temperate zone, thus calling into question multiple hypotheses that invoke faster tropical evolution to explain the latitudinal diversity gradient.

Asymmetric character displacement in mixed oak stands.

Ecological character displacement (ECD) refers to a pattern of increased divergence at sites where species ranges overlap caused by competition for resources. Although ECD is believed to be common, there are few in-depth studies that clearly establish its existence, especially in plants. Thus, we have compared leaf traits in allopatric and sympatric populations of two East Asian deciduous oaks: Quercus dentata and Quercus aliena. In contrast to previous studies, we define sympatry and allopatry at a local scale, thereby comparing populations that can or cannot directly interact. Using genetic markers, we found greater genetic divergence between the two oak species growing in mixed stands and inferred that long-term gene flow has predominantly occurred asymmetrically from the cold-tolerant species (Q. dentata) to the warm-demanding later colonizing species (Q. aliena). Analysis of leaf traits revealed greater divergence in mixed than in pure oak stands. This was mostly due to the later colonizing species being characterized by more resource-conservative traits in the presence of the other species. Controlling for relevant environmental differences did not alter these conclusions. These results suggest that asymmetric trait divergence can take place where species coexist, possibly due to the imbalance in demographic history of species resulting in asymmetric inter-specific selection pressures.

Hybridization fuelled diversification in Spialia butterflies.

The importance of hybridization and introgression is well documented in the evolution of plants but, in insects, their role is not fully understood. Given the fact that insects are the most diverse group of organisms, assessing the impact of reticulation events on their evolution may be key to comprehend the emergence of such remarkable diversity. Here, we used an insect model, the Spialia butterflies, to gather genomic evidence of hybridization as a promoter of novel diversity. By using double-digest RADseq (ddRADseq), we explored the phylogenetic relationships between Spialia orbifer, S. rosae and S. sertorius, and documented two independent events of interspecific gene flow. Our data support that the Iberian endemism S. rosae probably received genetic material from S. orbifer in both mitochondrial and nuclear DNA, which could have contributed to a shift in the ecological preferences of S. rosae. We also show that admixture between S. sertorius and S. orbifer probably occurred in Italy. As a result, the admixed Sicilian populations of S. orbifer are differentiated from the rest of populations both genetically and morphologically, and display signatures of reproductive character displacement in the male genitalia. Additionally, our analyses indicated that genetic material from S. orbifer is present in S. sertorius along the Italian Peninsula. Our findings add to the view that hybridization is a pervasive phenomenon in nature and in butterflies in particular, with important consequences for evolution due to the emergence of novel phenotypes.

What is adaptive radiation? Many manifestations of the phenomenon in an iconic lineage of Hawaiian spiders.

Adaptive radiation provides the ideal context for identifying and testing the processes that drive evolutionary diversification. However, different adaptive radiations show a variety of different patterns, making it difficult to come up with universal rules that characterize all such systems. Diversification may occur via several mechanisms including non-adaptive divergence, adaptation to novel environments, or character displacement driven by competition. Here, we characterize the ways these different drivers contribute to present-day diversity patterns, using the exemplary adaptive radiation of Hawaiian long-jawed orbweaver (Tetragnatha) spiders. We present the most taxonomically comprehensive phylogenetic hypothesis to date for this group, using 10 molecular markers and representatives from every known species across the archipelago. Among the lineages that make up this remarkable radiation, we find evidence for multiple diversification modalities. Several clades appear to have diversified in allopatry under a narrow range of ecological conditions, highlighting the role of niche conservatism in speciation. Others have shifted into new environments and evolved traits that appear to be adaptive in those environments. Still others show evidence for character displacement by close relatives, often resulting in convergent evolution of stereotyped ecomorphs. All of the above mechanisms seem to have played a role in giving rise to the exceptional diversity of morphological, ecological and behavioral traits represented among the many species of Hawaiian Tetragnatha. Taking all these processes into account, and testing how they operate in different systems, may allow us to identify universal principles underlying adaptive radiation.

Experimental test of selection against hybridization as a driver of avian signal divergence.

Signal divergence may be pivotal in the generation and maintenance of new biodiversity by allowing closely related species to avoid some costs of co-occurrence. In birds, closely related, sympatric species are more divergent in their colour patterns than those that live apart, but the selective pressures driving this pattern remain unclear. Traditionally, signal divergence among sympatric species is thought to result from selection against hybridization, but broad evidence is lacking. Here, we conducted field experiments on naïve birds using spectrometer-matched, painted 3D-printed models to test whether selection against hybridization drives colour pattern divergence in the genus Poecile. To address selection for male colour pattern divergence without the influence of learning or the evolution of female discrimination in sympatry, we simulated secondary contact between Poecile species, and conducted mate choice experiments on naïve, allopatric females. We found that female black-capped chickadees (Poecile atricapillus) are equally likely to perform copulation solicitation displays to sympatric and allopatric heterospecific congeners when they are paired with conspecifics, but exhibit a strong preference for less divergent males when presented with paired heterospecific congeners. These results suggest that increased colour pattern divergence among sympatric species can reduce the likelihood of mixed mating in some contexts, and therefore should be favoured by selection against hybridization.

A lot of convergence, a bit of divergence: Environment and interspecific interactions shape body colour patterns in Lissotriton newts.

Coexistence with related species poses evolutionary challenges to which populations may react in diverse ways. When exposed to similar environments, sympatric populations of two species may adopt similar phenotypic trait values. However, selection may also favour trait divergence as a way to reduce competition for resources or mates. The characteristics of external body parts, such as coloration and external morphology, are involved to varying degrees in intraspecific signalling as well as in the adaptation to the environment and consequently may be diversely affected by interspecific interactions in sympatry. Here, we studied the effect of sympatry on various colour and morphological traits in males and females of two related newt species Lissotriton helveticus and L. vulgaris. Importantly, we did not only estimate how raw trait differences between species respond to sympatry, but also the marginal responses after controlling for environmental variation. We found that dorsal and caudal coloration converged in sympatry, likely reflecting their role in adaptation to local environments, especially concealment from predators. In contrast, aspects of male and female ventral coloration, which harbours sexual signals in both species, diverged in sympatry. This divergence may reduce opportunities for interspecific sexual interactions and the associated loss of energy, suggesting reproductive character displacement (RCD). Our study emphasizes the contrasting patterns of traits involved in different functions and calls for the need to consider this diversity in evolutionary studies.

Context-dependent parasite infection affects trophic niche in populations of sympatric stickleback species.

How parasites alter host feeding ecology remains elusive in natural populations. A powerful approach to investigate the link between infection and feeding ecology is quantifying unique and shared responses to parasite infection in related host species within a common environment. Here, 9 pairs of sympatric populations of the three-spined and nine-spined stickleback fishes were sampled across a range of freshwater and brackish habitats to investigate how parasites alter host feeding ecology: (i) biotic and abiotic determinants of parasite community composition, and (ii) to what extent parasite infection correlates with trophic niche specialization of the 2 species, using stable isotope analyses (δ15N and δ13C). It was determined that parasite community composition and host parasite load varied among sites and species and were correlated with dissolved oxygen. It was also observed that the digenean Cyathocotyle sp.'s abundance, a common directly infecting parasite with a complex life cycle, correlated with host δ13C in a fish species-specific manner. In 6 sites, correlations were found between parasite abundance and their hosts' feeding ecology. These effects were location-specific and occasionally host species or host size-specific. Overall, the results suggest a relationship between parasite infection and host trophic niche which may be an important and largely overlooked ecological factor. The population specificity and variation in parasite communities also suggest this effect is multifarious and context-dependent.