Digest: Fossils,evolutionary models,and diatoms*

Adaptation to new environments by organisms has been and is of much interest in scientific research. Does the diatom lineage Stephanodiscus niagarae/yellowstonensis follow models compatible with adaptation to a new environment? Voje (2019) shows that in this lineage, none of the current models tested—decelerated evolution, Ornstein-Uhlenbeck, and random walk—fully explained how multiple traits—valve diameter, the number of costae, and spines per valve—evolved. More accurate models are needed to understand the evolutionary history of these diatoms.     

USE OF RIBOSOMAL DNA INTERNAL TRANSCRIBED SPACERS FOR PHYLOGENETIC STUDIES IN DIATOMS1

Sequence variation of ribosomal DNA internal transcribed spacers (ITS) among populations, species, and genera of the diatom genus Stephanodiscus was investigated. ITS 1 and ITS 2, including the 5.8S gene, were sequenced from geographically distant and nearby populations of S. niagarae Ehrenberg. In addition, repeats from S. hantzschii Grunow and Cyclotella meneghiniana Kützing were sequenced to determine the taxonomic range over which the ITS region could be used for diatom systematics. The morphologically distinct S. yellowstonensis Theriot & Stoermer, thought to have evolved from S. niagarae in Yellowstone Lake between 12,000 and 8000 years ago, also was sequenced to assess its relationship to nearby S. niagarae populations. The organization and relative sizes of ITS 1 and ITS 2 in Stephanodiscus species were similar to those reported for other eukaryotes. In general, ITS 2 was slightly larger and more variable than ITS 1. Cladistic analysis of ITS sequences did not resolve relationships of nearby S. niagarae and S. yellowstonensis populations. However, central North American S. niagarae populations were in a clade supported by two nucleotide changes. For Cyclotella, much of the ITS region was not alignable with that for Stephanodiscus species; therefore, generic-level comparison within the Thalassiosiraceae may not be possible. The variation (95–96% similarity) between S. hantzschii and other Stephanodiscus species suggests that interspecific relationships could be assessed with ITS sequences. Although S. yellowstonensis is morphologically distinct from S. niagarae, no autapomorphic nucleotide sites were identified. Two S. niagarae populations (Heart and Lewis Lakes), however, did possess autapomorphic ITS sites.     

Adaptive landscape and functional diversity of Neotropical cichlids: implications for the ecology and evolution of Cichlinae (Cichlidae; Cichliformes)

Morphological, lineage and ecological diversity can vary substantially even among closely related lineages. Factors that influence morphological diversification, especially in functionally relevant traits, can help to explain the modern distribution of disparity across phylogenies and communities. Multivariate axes of feeding functional morphology from 75 species of Neotropical cichlid and a stepwise‐AIC algorithm were used to estimate the adaptive landscape of functional morphospace in Cichlinae. Adaptive landscape complexity and convergence, as well as the functional diversity of Cichlinae, were compared with expectations under null evolutionary models. Neotropical cichlid feeding function varied primarily between traits associated with ram feeding vs. suction feeding/biting and secondarily with oral jaw muscle size and pharyngeal crushing capacity. The number of changes in selective regimes and the amount of convergence between lineages was higher than expected under a null model of evolution, but convergence was not higher than expected under a similarly complex adaptive landscape. Functional disparity was compatible with an adaptive landscape model, whereas the distribution of evolutionary change through morphospace corresponded with a process of evolution towards a single adaptive peak. The continentally distributed Neotropical cichlids have evolved relatively rapidly towards a number of adaptive peaks in functional trait space. Selection in Cichlinae functional morphospace is more complex than expected under null evolutionary models. The complexity of selective constraints in feeding morphology has likely been a significant contributor to the diversity of feeding ecology in this clade.     

Evolution toward a new adaptive optimum: phenotypic evolution in a fossil stickleback lineage

Natural selection has almost certainly shaped many evolutionary trajectories documented in fossil lineages, but it has proven difficult to demonstrate this claim by analyzing sequences of evolutionary changes. In a recently published and particularly promising test case, an evolutionary time series of populations displaying armor reduction in a fossil stickleback lineage could not be consistently distinguished from a null model of neutral drift, despite excellent temporal resolution and an abundance of indirect evidence implicating natural selection. Here, we revisit this case study, applying analyses that differ from standard approaches in that: (1) we do not treat genetic drift as a null model, and instead assess neutral and adaptive explanations on equal footing using the Akaike Information Criterion; and (2) rather than constant directional selection, the adaptive scenario we consider is that of a population ascending a peak on the adaptive landscape, modeled as an Orstein-Uhlenbeck process. For all three skeletal features measured in the stickleback lineage, the adaptive model decisively outperforms neutral evolution, supporting a role for natural selection in the evolution of these traits. These results demonstrate that, at least under favorable circumstances, it is possible to infer in fossil lineages the relationship between evolutionary change and features of the adaptive landscape.     

Evolutionary Distributions and Competition by Way of Reaction-Diffusion and by Way of Convolution

Evolution by natural selection is the most ubiquitous and well understood process of evolution. We say distribution instead of the distribution of the density of populations of phenotypes across the values of their adaptive traits. A phenotype refers to an organism that exhibits a set of values of adaptive traits. An adaptive trait is a trait that a phenotype exhibits where the trait is subject to natural selection. Natural selection is a process by which populations of different phenotypes decline at different rates. An evolutionary distribution (ED) encapsulates the dynamics of evolution by natural selection. The main results are: (i) ED are derived by way of PDE of reaction-diffusion type and by way of integro-differential equations. The latter capture mutations through convolution of a kernel with the rate of growth of a population. The kernel controls the size and rate of mutations. (ii) The numerical solution of a logistic-like ED driven by competition corresponds to a bounded traveling wave solution of population models based on the logistic. (iii) Competition leads to increase in diversity of phenotypes on a single ED. Diversity refers to change in the number of local maxima (minima) within the bounds of values of adaptive traits. (iv) The principle of competitive exclusion in the context of evolution depends, smoothly, on the size and rate of mutations. (v) We identify the sensitivity—with respect to survival—of phenotypes to changes in values of adaptive traits to be an important parameter: increase in the value of this parameter results in decrease in evolutionary-based diversity. (vi) Stable ED corresponds to Evolutionary Stable Strategy; the latter refers to the outcome of a game of evolution.     

Social runaway: Fisherian elaboration (or reduction) of socially selected traits via indirect genetic effects

Our understanding of the evolutionary stability of socially selected traits is dominated by sexual selection models originating with R. A. Fisher, in which genetic covariance arising through assortative mating can trigger exponential, runaway trait evolution. To examine whether nonreproductive, socially selected traits experience similar dynamics—social runaway—when assortative mating does not automatically generate a covariance, we modeled the evolution of socially selected badge and donation phenotypes incorporating indirect genetic effects (IGEs) arising from the social environment. We establish a social runaway criterion based on the interaction coefficient, ψ , which describes social effects on badge and donation traits. Our models make several predictions. (1) IGEs can drive the original evolution of altruistic interactions that depend on receiver badges. (2) Donation traits are more likely to be susceptible to IGEs than badge traits. (3) Runaway dynamics in nonsexual, social contexts can occur in the absence of a genetic covariance. (4) Traits elaborated by social runaway are more likely to involve reciprocal, but nonsymmetrical, social plasticity. Models incorporating plasticity to the social environment via IGEs illustrate conditions favoring social runaway, describe a mechanism underlying the origins of costly traits, such as altruism, and support a fundamental role for phenotypic plasticity in rapid social evolution.     

Tempo and mode of performance evolution across multiple independent origins of adhesive toe pads in lizards

Understanding macroevolutionary dynamics of trait evolution is an important endeavor in evolutionary biology. Ecological opportunity can liberate a trait as it diversifies through trait space, while genetic and selective constraints can limit diversification. While many studies have examined the dynamics of morphological traits, diverse morphological traits may yield the same or similar performance and as performance is often more proximately the target of selection, examining only morphology may give an incomplete understanding of evolutionary dynamics. Here, we ask whether convergent evolution of pad‐bearing lizards has followed similar evolutionary dynamics, or whether independent origins are accompanied by unique constraints and selective pressures over macroevolutionary time. We hypothesized that geckos and anoles each have unique evolutionary tempos and modes. Using performance data from 59 species, we modified Brownian motion (BM) and Ornstein–Uhlenbeck (OU) models to account for repeated origins estimated using Bayesian ancestral state reconstructions. We discovered that adhesive performance in geckos evolved in a fashion consistent with Brownian motion with a trend, whereas anoles evolved in bounded performance space consistent with more constrained evolution (an Ornstein–Uhlenbeck model). Our results suggest that convergent phenotypes can have quite distinctive evolutionary patterns, likely as a result of idiosyncratic constraints or ecological opportunities.     

Measuring the contribution of evolution to community trait structure in freshwater zooplankton

There are currently few predictions about when evolutionary processes are likely to play an important role in structuring community features. Determining predictors that indicate when evolution is expected to impact ecological processes in natural landscapes can help researchers identify eco-evolutionary ‘hotspots', where eco-evolutionary interactions are more likely to occur. Using data collected from a survey in freshwater cladoceran communities, landscape population genetic data and phenotypic trait data measured in a common garden, we applied a Bayesian linear model to assess whether the impact of local trait evolution in the keystone species Daphnia magna on cladoceran community trait values could be predicted by population genetic properties (within-population genetic diversity, genetic distance among populations), ecological properties (Simpson's diversity, phenotypic divergence) or environmental divergence. We found that the impact of local trait evolution varied among communities. Moreover, community diversity and phenotypic divergence were found to be better predictors of the contribution of evolution to community trait values than environmental features or genetic properties of the evolving species. Our results thus indicate the importance of ecological context for the impact of evolution on community features. Our study also demonstrates one way to detect signatures of eco-evolutionary interactions in communities inhabiting heterogeneous landscapes using survey data of contemporary ecological and evolutionary structure.     

Symmetric competition as a general model for single-species adaptive dynamics

Adaptive dynamics is a widely used framework for modeling long-term evolution of continuous phenotypes. It is based on invasion fitness functions, which determine selection gradients and the canonical equation of adaptive dynamics. Even though the derivation of the adaptive dynamics from a given invasion fitness function is general and model-independent, the derivation of the invasion fitness function itself requires specification of an underlying ecological model. Therefore, evolutionary insights gained from adaptive dynamics models are generally model-dependent. Logistic models for symmetric, frequency-dependent competition are widely used in this context. Such models have the property that the selection gradients derived from them are gradients of scalar functions, which reflects a certain gradient property of the corresponding invasion fitness function. We show that any adaptive dynamics model that is based on an invasion fitness functions with this gradient property can be transformed into a generalized symmetric competition model. This provides a precise delineation of the generality of results derived from competition models. Roughly speaking, to understand the adaptive dynamics of the class of models satisfying a certain gradient condition, one only needs a complete understanding of the adaptive dynamics of symmetric, frequency-dependent competition. We show how this result can be applied to number of basic issues in evolutionary theory.     

Functional performance of turtle humerus shape across an ecological adaptive landscape

The concept of the adaptive landscape has been invaluable to evolutionary biologists for visualizing the dynamics of selection and adaptation, and is increasingly being used to study morpho‐functional data. Here, we construct adaptive landscapes to explore functional trade‐offs associated with variation in humerus morphology among turtles adapted to three different locomotor environments: marine, semiaquatic, and terrestrial. Humerus shape from 40 species of cryptodire turtles was quantified using a pseudolandmark approach. Hypothetical shapes were extracted in a grid across morphospace and four functional traits (strength, stride length, mechanical advantage, and hydrodynamics) measured on those shapes. Quantitative trait modeling was used to construct adaptive landscapes that optimize the functional traits for each of the three locomotor ecologies. Our data show that turtles living in different environments have statistically different humeral shapes. The optimum adaptive landscape for each ecology is defined by a different combination of performance trade‐offs, with turtle species clustering around their respective adaptive peak. Further, species adhere to pareto fronts between marine–semiaquatic and semiaquatic–terrestrial optima, but not between marine–terrestrial. Our study demonstrates the utility of adaptive landscapes in informing the link between form, function, and ecological adaptation, and establishes a framework for reconstructing turtle ecological evolution using isolated humeri from the fossil record.     

AN ADAPTIVE RADIATION OF FROGS IN A SOUTHEAST ASIAN ISLAND ARCHIPELAGO

Living amphibians exhibit a diversity of ecologies, life histories, and species‐rich lineages that offers opportunities for studies of adaptive radiation. We characterize a diverse clade of frogs (Kaloula, Microhylidae) in the Philippine island archipelago as an example of an adaptive radiation into three primary habitat specialists or ecotypes. We use a novel phylogenetic estimate for this clade to evaluate the tempo of lineage accumulation and morphological diversification. Because species‐level phylogenetic estimates for Philippine Kaloula are lacking, we employ dense population sampling to determine the appropriate evolutionary lineages for diversification analyses. We explicitly take phylogenetic uncertainty into account when calculating diversification and disparification statistics and fitting models of diversification. Following dispersal to the Philippines from Southeast Asia, Kaloula radiated rapidly into several well‐supported clades. Morphological variation within Kaloula is partly explained by ecotype and accumulated at high levels during this radiation, including within ecotypes. We pinpoint an axis of morphospace related directly to climbing and digging behaviors and find patterns of phenotypic evolution suggestive of ecological opportunity with partitioning into distinct habitat specialists. We conclude by discussing the components of phenotypic diversity that are likely important in amphibian adaptive radiations.     

Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation

Adaptive diversification is thought to be shaped by ecological opportunity. A prediction of this ecological process of diversification is that it should result in congruent bursts of lineage and phenotypic diversification, but few studies have found this expected association. Here, we study the relationship between rates of lineage diversification and body size evolution in the turtle ants, a diverse Neotropical clade. Using a near complete, time‐calibrated phylogeny we investigated lineage diversification dynamics and body size disparity through model fitting analyses and estimation of per‐lineage rates of cladogenesis and phenotypic evolution. We identify an exceptionally high degree of congruence between the high rates of lineage and body size diversification in a young clade undergoing renewed diversification in the ecologically distinct Chacoan biogeographical region of South America. It is likely that the region presented turtle ants with novel ecological opportunity, which facilitated a nested burst of diversification and phenotypic evolution within the group. Our results provide a compelling quantitative example of tight congruence between rates of lineage and phenotypic diversification, meeting the key predicted pattern of adaptive diversification shaped by ecological opportunity.     

Fluctuation domains in adaptive evolution

We derive an expression for the variation between parallel trajectories in phenotypic evolution, extending the well known result that predicts the mean evolutionary path in adaptive dynamics or quantitative genetics. We show how this expression gives rise to the notion of fluctuation domains-parts of the fitness landscape where the rate of evolution is very predictable (due to fluctuation dissipation) and parts where it is highly variable (due to fluctuation enhancement). These fluctuation domains are determined by the curvature of the fitness landscape. Regions of the fitness landscape with positive curvature, such as adaptive valleys or branching points, experience enhancement. Regions with negative curvature, such as adaptive peaks, experience dissipation. We explore these dynamics in the ecological scenarios of implicit and explicit competition for a limiting resource.     

The adaptive dynamics of niche constructing traits in spatially subdivided populations: evolving posthumous extended phenotypes

Niche construction, by which organisms modify the environment in which they live, has been proposed to affect the evolution of many phenotypic traits. But what about the evolution of a niche constructing trait itself, whose expression changes the pattern of natural selection to which the trait is exposed in subsequent generations? This article provides an inclusive fitness analysis of selection on niche constructing phenotypes, which can affect their environment from local to global scales in arbitrarily spatially subdivided populations. The model shows that phenotypic effects of genes extending far beyond the life span of the actor can be affected by natural selection, provided they modify the fitness of those individuals living in the future that are likely to have inherited the niche construction lineage of the actor. Present benefits of behaviors are thus traded off against future indirect costs. The future costs will generally result from a complicated interplay of phenotypic effects, population demography and environmental dynamics. To illustrate these points, I derive the adaptive dynamics of a trait involved in the consumption of an abiotic resource, where resource abundance in future generations feeds back to the evolutionary dynamics of the trait.     

Ecological opportunity and the origin of adaptive radiations

Ecological opportunity – through entry into a new environment, the origin of a key innovation or extinction of antagonists – is widely thought to link ecological population dynamics to evolutionary diversification. The population‐level processes arising from ecological opportunity are well documented under the concept of ecological release. However, there is little consensus as to how these processes promote phenotypic diversification, rapid speciation and adaptive radiation. We propose that ecological opportunity could promote adaptive radiation by generating specific changes to the selective regimes acting on natural populations, both by relaxing effective stabilizing selection and by creating conditions that ultimately generate diversifying selection. We assess theoretical and empirical evidence for these effects of ecological opportunity and review emerging phylogenetic approaches that attempt to detect the signature of ecological opportunity across geological time. Finally, we evaluate the evidence for the evolutionary effects of ecological opportunity in the diversification of Caribbean Anolis lizards. Some of the processes that could link ecological opportunity to adaptive radiation are well documented, but others remain unsupported. We suggest that more study is required to characterize the form of natural selection acting on natural populations and to better describe the relationship between ecological opportunity and speciation rates.     

Thermodynamical interpretation of evolutionary dynamics on a fitness landscape in an evolution reactor,II

In our previous report [Aita, T., Morinaga, S., Hosimi, Y., 2004. Thermodynamical interpretation of evolutionary dynamics on a fitness landscape in an evolution reactor I. Bull. Math. Biol. 66, 1371–1403], an analogy between thermodynamics and adaptive walks on a Mt. Fuji-type fitness landscape in an artificial selection system was presented. Introducing the ‘free fitness’ as the sum of a fitness term and an entropy term and ‘evolutionary force’ as the gradient of free fitness on a fitness coordinate, we demonstrated that the adaptive walk (=evolution) is driven by the evolutionary force in the direction in which free fitness increases. In this report, we examine the effect of various modifications of the original model on the properties of the adaptive walk. The modifications were as follows: first, mutation distance d was distributed obeying binomial distribution; second, the selection process obeyed the natural selection protocol; third, ruggedness was introduced to the landscape according to the NK model; fourth, a noise was included in the fitness measurement. The effect of each modification was described in the same theoretical framework as the original model by introducing ‘effective’ quantities such as the effective mutation distance or the effective screening size.     

Shared human-chimpanzee pattern of perinatal femoral shaft morphology and its implications for the evolution of hominin locomotor adaptations

Background

Acquisition of bipedality is a hallmark of human evolution. How bipedality evolved from great ape-like locomotor behaviors, however, is still highly debated. This is mainly because it is difficult to infer locomotor function, and even more so locomotor kinematics, from fossil hominin long bones. Structure-function relationships are complex, as long bone morphology reflects phyletic history, developmental programs, and loading history during an individual’s lifetime. Here we discriminate between these factors by investigating the morphology of long bones in fetal and neonate great apes and humans, before the onset of locomotion.

Methodology/Principal Findings

Comparative morphometric analysis of the femoral diaphysis indicates that its morphology reflects phyletic relationships between hominoid taxa to a greater extent than taxon-specific locomotor adaptations. Diaphyseal morphology in humans and chimpanzees exhibits several shared-derived features, despite substantial differences in locomotor adaptations. Orangutan and gorilla morphologies are largely similar, and likely represent the primitive hominoid state.

Conclusions/Significance

These findings are compatible with two possible evolutionary scenarios. Diaphyseal morphology may reflect retained adaptive traits of ancestral taxa, hence human-chimpanzee shared-derived features may be indicative of the locomotor behavior of our last common ancestor. Alternatively, diaphyseal morphology might reflect evolution by genetic drift (neutral evolution) rather than selection, and might thus be more informative about phyletic relationships between taxa than about locomotor adaptations. Both scenarios are consistent with the hypothesis that knuckle-walking in chimpanzees and gorillas resulted from convergent evolution, and that the evolution of human bipedality is unrelated to extant great ape locomotor specializations.     

Gillespie eco‐evolutionary models (GEMs) reveal the role of heritable trait variation in eco‐evolutionary dynamics

Heritable trait variation is a central and necessary ingredient of evolution. Trait variation also directly affects ecological processes, generating a clear link between evolutionary and ecological dynamics. Despite the changes in variation that occur through selection, drift, mutation, and recombination, current eco‐evolutionary models usually fail to track how variation changes through time. Moreover, eco‐evolutionary models assume fitness functions for each trait and each ecological context, which often do not have empirical validation. We introduce a new type of model, Gillespie eco‐evolutionary models (GEMs), that resolves these concerns by tracking distributions of traits through time as eco‐evolutionary dynamics progress. This is done by allowing change to be driven by the direct fitness consequences of model parameters within the context of the underlying ecological model, without having to assume a particular fitness function. GEMs work by adding a trait distribution component to the standard Gillespie algorithm – an approach that models stochastic systems in nature that are typically approximated through ordinary differential equations. We illustrate GEMs with the Rosenzweig–MacArthur consumer–resource model. We show not only how heritable trait variation fuels trait evolution and influences eco‐evolutionary dynamics, but also how the erosion of variation through time may hinder eco‐evolutionary dynamics in the long run. GEMs can be developed for any parameter in any ordinary differential equation model and, furthermore, can enable modeling of multiple interacting traits at the same time. We expect GEMs will open the door to a new direction in eco‐evolutionary and evolutionary modeling by removing long‐standing modeling barriers, simplifying the link between traits, fitness, and dynamics, and expanding eco‐evolutionary treatment of a greater diversity of ecological interactions. These factors make GEMs much more than a modeling advance, but an important conceptual advance that bridges ecology and evolution through the central concept of heritable trait variation.     

ADAPTIVE EVOLUTION OF PLASTRON SHAPE IN EMYDINE TURTLES

Morphology reflects ecological pressures, phylogeny, and genetic and biophysical constraints. Disentangling their influence is fundamental to understanding selection and trait evolution. Here, we assess the contributions of function, phylogeny, and habitat to patterns of plastron (ventral shell) shape variation in emydine turtles. We quantify shape variation using geometric morphometrics, and determine the influence of several variables on shape using path analysis. Factors influencing plastron shape variation are similar between emydine turtles and the more inclusive Testudinoidea. We evaluate the fit of various evolutionary models to the shape data to investigate the selective landscape responsible for the observed morphological patterns. The presence of a hinge on the plastron accounts for most morphological variance, but phylogeny and habitat also correlate with shape. The distribution of shape variance across emydine phylogeny is most consistent with an evolutionary model containing two adaptive zones—one for turtles with kinetic plastra, and one for turtles with rigid plastra. Models with more complex adaptive landscapes often fit the data only as well as the null model (purely stochastic evolution). The adaptive landscape of plastron shape in Emydinae may be relatively simple because plastral kinesis imposes overriding mechanical constraints on the evolution of form.