Wiley: Evolution: Table of Contents

Public good‐driven release of heterogeneous resources leads to genotypic diversification of an isogenic yeast population

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Understanding the basis of biological diversity remains a central problem in evolutionary biology. Using microbial systems, adaptive diversification has been studied in (a) spatially heterogeneous environments, (b) temporally segregated resources, and (c) resource specialization in a homogeneous environment. However, it is not well understood how adaptive diversification can take place in a homogeneous environment containing a single resource. Starting from an isogenic population of yeast Saccharomyces cerevisiae, we report rapid adaptive diversification, when propagated in an environment containing melibiose as the carbon source. The diversification is driven due to a public good enzyme α-galactosidase, which hydrolyzes melibiose into glucose and galactose. The diversification is driven by mutations at a single locus, in the GAL3 gene in the S. cerevisiae GAL/MEL regulon. We show that metabolic co-operation involving public resources could be an important mode of generating biological diversity. Our study demonstrates sympatric diversification of yeast starting from an isogenic population and provides detailed mechanistic insights into the factors and conditions responsible for generating and maintaining the population diversity.

The spatial scale of adaptation in a native annual plant and its implications for responses to climate change

Amanda J. Gorton, John W. Benning, Peter Tiffin, David A. Moeller — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Spatial patterns of adaptation provide important insights into agents of selection and expected responses of populations to climate change. Robust inference into the spatial scale of adaptation can be gained through reciprocal transplant experiments that combine multiple source populations and common gardens. Here, we examine the spatial scale of local adaptation of the North American annual plant common ragweed, Ambrosia artemisiifolia, using data from four common gardens with 22 source populations sampled from across a ∼1200 km latitudinal gradient within the native range. We found evidence of local adaptation at the northernmost common garden, but maladaptation at the two southern gardens, where more southern source populations outperformed local populations. Overall, the spatial scale of adaptation was large—at the three gardens where distance between source populations and gardens explained variation in fitness, it took an average of 820 km for fitness to decline to 50% of its predicted maximum. Taken together, these results suggest that climate change has already caused maladaptation, especially across the southern portion of the range, and may result in northward range contraction over time.

Multigenerational downregulation of insulin/IGF‐1 signaling in adulthood improves lineage survival, reproduction, and fitness in Caenorhabditis elegans supporting the developmental theory of ageing

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Adulthood-only downregulation of insulin/IGF-1 signaling (IIS), an evolutionarily conserved pathway regulating resource allocation between somatic maintenance and reproduction, increases life span without fecundity cost in the nematode, Caenorhabditis elegans. However, long-term multigenerational effects of reduced IIS remain unexplored and are proposed to carry costs for offspring quality. To test this hypothesis, we ran a mutation accumulation (MA) experiment and downregulated IIS in half of the 400 MA lines by silencing daf-2 gene expression using RNA interference (RNAi) across 40 generations. Contrary to the prediction, adulthood-only daf-2 RNAi reduced extinction of MA lines both under UV-induced and spontaneous MA. Fitness of the surviving UV-induced MA lines was higher under daf-2 RNAi. Reduced IIS increased intergenerational F1 offspring fitness under UV stress but had no quantifiable transgenerational effects. Functional hrde-1 was required for the benefits of multigenerational daf-2 RNAi. Overall, we found net benefit to fitness from multigenerational reduction of IIS and the benefits became more apparent under stress. Because reduced daf-2 expression during development carries fitness costs, we suggest that our findings are best explained by the developmental theory of ageing, which maintains that the decline in the force of selection with age results in poorly regulated gene expression in adulthood.

The evolution of sex similarities in social signals: Climatic seasonality is associated with lower sexual dimorphism and greater elaboration of female and male signals in antbirds (Thamnophilidae)

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Selection on signals that mediate social competition varies with resource availability. Climate regulates resource availability, which may affect the strength of competition and selection on signals. Traditionally, this meant that more seasonal, colder, or dryer—overall harsher—environments should favor the elaboration of male signals under stronger male-male competition, increasing sexual dimorphism. However, females also use signals to compete; thus, harsher environments could strengthen competition and favor elaboration of signals in both sexes, decreasing sexual dimorphism. Alternatively, harsher environments could decrease sexual dimorphism due to scarcer resources to invest in signal elaboration in both sexes. We evaluated these contrasting hypotheses in antbirds, a family of Neotropical passerines that varies in female and male signals and occurs across diverse climatic regimes. We tested the association of sexual dimorphism of plumage coloration and songs with temperature, precipitation, and their seasonality. We found that greater seasonality is associated with lower sexual dimorphism in plumage coloration and greater elaboration of visual signals in both sexes, but not acoustic signals. Our results suggest that greater seasonality may be associated with convergent elaboration of female and male visual signals, highlighting the role of signals of both sexes in the evolution of sexual dimorphism.

Macroevolutionary patterns in marine hermaphroditism

George C. Jarvis, Craig R. White, Dustin J. Marshall — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Most plants and many animals are hermaphroditic; whether the same forces are responsible for hermaphroditism in both groups is unclear. The well-established drivers of hermaphroditism in plants (e.g., seed dispersal potential, pollination mode) have analogues in animals (e.g., larval dispersal potential, fertilization mode), allowing us to test the generality of the proposed drivers of hermaphroditism across both groups. Here, we test these theories for 1153 species of marine invertebrates, from three phyla. Species with either internal fertilization, restricted offspring dispersal, or small body sizes are more likely to be hermaphroditic than species that are external fertilizers, planktonic developers, or larger. Plants and animals show different biogeographical patterns, however: animals are less likely to be hermaphroditic at higher latitudes—the opposite to the trend in plants. Overall, our results suggest that similar forces, namely, competition among offspring or gametes, shape the evolution of hermaphroditism across plants and three invertebrate phyla.

Plant phenotypic plasticity changes pollinator‐mediated selection

Thomas Dorey, Florian P. Schiestl — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Many organisms change their phenotype in response to the environment, a phenomenon called phenotypic plasticity. Although plasticity can dramatically change the phenotype of an organism, we hardly understand how this can affect biotic interactions and the resulting phenotypic selection. Here, we use fast cycling Brassica rapa plants in an experiment in the greenhouse to study the link between plasticity and selection. We detected strong plasticity in morphology, nectar, and floral scent in response to different soil types and aphid herbivory. We found positive selection on nectar and morphological traits in hand- and bumblebee-pollinated plants. Bumblebee-mediated selection on a principal component representing plant height, flower number, and flowering time (mPC3) differed depending on soil type and herbivory. For plants growing in richer soil, selection was stronger in the absence of herbivores, whereas for plants growing in poorer soil selection was stronger with herbivory. We showed that bumblebees visited tall plants with many flowers overproportionally in plants in poor soil with herbivory (i.e., when tall plants were rare), thus causing stronger positive selection on this trait combination. We suggest that with strong plasticity under most stressful conditions, pollinator-mediated selection may promote adaptation to local environmental factors given sufficient heritability of the traits under selection.

Why are animals conspicuously colored? Evolution of sexual versus warning signals in land vertebrates

Zachary Emberts, John J. Wiens — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Conspicuous colors (e.g., red, yellow, blue) have evolved numerous times across animals. But the function of this coloration can differ radically among species. Many species use this coloration as a sexual signal to conspecifics, whereas others use it as a warning signal to predators. Why do different species evolve conspicuous coloration in association with one function as opposed to the other? We address this question in terrestrial vertebrates (tetrapods) using phylogenetic approaches, and test whether day-night activities of species help determine these patterns. Using phylogenetic logistic regression, we found that conspicuous, sexually dimorphic coloration is significantly associated with diurnal lineages (e.g., many birds and lizards). By contrast, the evolution of warning signals was significantly associated with large-scale clades that were ancestrally nocturnal (e.g., snakes, amphibians), regardless of the current diel activity of species. Overall, we show that the evolution of conspicuous coloration as warning signals or sexual signals is influenced by the ecology of species, both recently and in the ancient past.

The anteriorization of tooth position underlies the atavism of tooth morphology: Insights into the morphogenesis of mammalian molars

Tomohiro Harano, Masakazu Asahara — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

The evolution and development of complex molars as a key innovation in mammals have long been of interest yet remain poorly understood. With reference to century-old theories and modern findings, we focused on the teeth of pinnipeds (Carnivora) and cetaceans (Cetartiodactyla), which are morphologically simple compared with those of other mammals, and thus can be considered a reversal toward the ancestral state of nonmammalian synapsids. By reconstructing the evolutionary history of tooth complexity for the phylogenies of Carnivora and Cetartiodactyla, we established that a secondary evolution of simple teeth from more complex molars has occurred independently multiple times. Our phylogenetic comparative analyses showed that a simplification in tooth morphology was correlated with a more anterior dentition position relative to the component bones of the upper jaw in both Carnivora and Cetartiodactyla. These results suggest that the anterior shift of tooth position relative to the morphogenetic fields present in the jaw contributed to the evolutionary simplification in molar morphology. Our findings provide insights into the developmental basis of complex mammalian dentition.

Decoupled evolution of the cranium and mandible in carnivoran mammals

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

The relationship between skull morphology and diet is a prime example of adaptive evolution. In mammals, the skull consists of the cranium and the mandible. Although the mandible is expected to evolve more directly in response to dietary changes, dietary regimes may have less influence on the cranium because additional sensory and brain-protection functions may impose constraints on its morphological evolution. Here, we tested this hypothesis by comparing the evolutionary patterns of cranium and mandible shape and size across 100+ species of carnivoran mammals with distinct feeding ecologies. Our results show decoupled modes of evolution in cranial and mandibular shape; cranial shape follows clade-based evolutionary shifts, whereas mandibular shape evolution is linked to broad dietary regimes. These results are consistent with previous hypotheses regarding hierarchical morphological evolution in carnivorans and greater evolutionary lability of the mandible with respect to diet. Furthermore, in hypercarnivores, the evolution of both cranial and mandibular size is associated with relative prey size. This demonstrates that dietary diversity can be loosely structured by craniomandibular size within some guilds. Our results suggest that mammal skull morphological evolution is shaped by mechanisms beyond dietary adaptation alone.

Laplace's demon in biology: Models of evolutionary prediction

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Our ability to predict natural phenomena can be limited by incomplete information. This issue is exemplified by “Laplace's demon,” an imaginary creature proposed in the 18th century, who knew everything about everything, and thus could predict the full nature of the universe forward or backward in time. Quantum mechanics, among other things, has cast doubt on the possibility of Laplace's demon in the full sense, but the idea still serves as a useful metaphor for thinking about the extent to which prediction is limited by incomplete information on deterministic processes versus random factors. Here, we use simple analytical models and computer simulations to illustrate how data limits can be captured in a Bayesian framework, and how they influence our ability to predict evolution. We show how uncertainty in measurements of natural selection, or low predictability of external environmental factors affecting selection, can greatly reduce predictive power, often swamping the influence of intrinsic randomness caused by genetic drift. Thus, more accurate knowledge concerning the causes and action of natural selection is key to improving prediction. Fortunately, our analyses and simulations show quantitatively that reasonable improvements in data quantity and quality can meaningfully increase predictability.

The diverse effects of phenotypic dominance on hybrid fitness

Hilde Schneemann, Aslı D. Munzur, Ken A. Thompson, John J. Welch — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

When divergent populations interbreed, their alleles are brought together in hybrids. In the initial F1 cross, most divergent loci are heterozygous. Therefore, F1 fitness can be influenced by dominance effects that could not have been selected to function well together. We present a systematic study of these F1 dominance effects by introducing variable phenotypic dominance into Fisher's geometric model. We show that dominance often reduces hybrid fitness, which can generate optimal outbreeding followed by a steady decline in F1 fitness, as is often observed. We also show that “lucky” beneficial effects sometimes arise by chance, which might be important when hybrids can access novel environments. We then show that dominance can lead to violations of Haldane's Rule (reduced fitness of the heterogametic F1) but strengthens Darwin's Corollary (F1 fitness differences between cross directions). Taken together, results show that the effects of dominance on hybrid fitness can be surprisingly difficult to isolate, because they often resemble the effects of uniparental inheritance or expression. Nevertheless, we identify a pattern of environment-dependent heterosis that only dominance can explain, and for which there is some suggestive evidence. Our results also show how existing data set upper bounds on the size of dominance effects. These bounds could explain why additive models often provide good predictions for later-generation recombinant hybrids, even when dominance qualitatively changes outcomes for the F1.

Evolutionary loss of shell pigmentation, pattern, and eye structure in deep‐sea snails in the dysphotic zone

Suzanne T. Williams, Emily S. Noone, Lisa Marie Smith, Lauren Sumner‐Rooney — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Adaptations to habitats lacking light, such as the reduction or loss of eyes and pigmentation, have fascinated biologists for centuries, yet have rarely been studied in the deep sea, the earth's oldest and largest light-limited habitat. Here, we investigate the evolutionary loss of shell pigmentation, pattern, and eye structure across a family of deep-sea gastropods (Solariellidae). We show that within our phylogenetic framework, loss of these traits evolves without reversal, at different rates (faster for shell traits than eye structure), and over different depth ranges. Using a Bayesian approach, we find support for correlated evolution of trait loss with increasing depth within the dysphotic region. A transition to trait loss occurs for pattern and eye structure at 400–500 m and for pigmentation at 600–700 m. We also show that one of the sighted, shallow-water species, Ilanga navakaensis, which may represent the “best-case” scenario for vision for the family, likely has poor spatial acuity and contrast sensitivity. We therefore propose that pigmentation and pattern are not used for intraspecific communication but are important for camouflage from visual predators, and that the low-resolution vision of solariellids is likely to require high light intensity for basic visual tasks, such as detecting predators.

Herbivory modifies plant symbiont number and impact on host plant performance in the field

Steven T. Cassidy, Shaniya Markalanda, Connor J. McFadden, Corlett W. Wood — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Species interactions are a unifying theme in ecology and evolution. Both fields are currently moving beyond their historical focus on isolated pairwise relationships to understand how ecological communities affect focal interactions. Additional species can modify both the number of interactions and the fitness consequences of each interaction (i.e., selection). Although only selection affects the evolution of the focal interaction, the two are often conflated, limiting our understanding of the evolution of multispecies interactions. We manipulated aboveground herbivory on the legume Medicago lupulina in the field and quantified its effect on number of symbionts and the per-symbiont impact on plant performance in two belowground symbioses: mutualistic rhizobia bacteria (Ensifer meliloti) and parasitic root-knot nematodes (Meloidogyne hapla). We found that herbivores modified the number of rhizobia nodules, as well as the benefit per nodule. However, each effect was specific to a distinct herbivory regime: natural herbivory affected nodule number, whereas leafhoppers (Cicadellidae) weakened the per nodule benefit. We did not detect any effect of herbivory on nematode gall number or the cost of infection. Our data demonstrate that distinguishing between symbiont number from the fitness consequences of symbiosis is crucial to accurately infer how pairwise interactions will evolve in a community.

Influence of microhabitat, fecundity, and parental care on the evolution of sexual size dimorphism in Caribbean Eleutherodactylus frogs

Alvaro Dugo‐Cota, Carles Vilà, Ariel Rodríguez, Alejandro Gonzalez‐Voyer — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Rensch's rule suggests that sexual size dimorphism (SSD) increases with species size when males are the larger sex, whereas it decreases when females are the larger sex. However, the process responsible for this pattern remains obscure. SSD can result from sexual selection, such as intrasexual competition for access to mates, or from natural selection, due to resource partitioning or fecundity selection. We studied SSD in Caribbean Eleutherodactylus frogs using phylogenetic comparative methods to investigate the influence of microhabitat, fecundity, and parental care. Our results show that in Caribbean Eleutherodactylus females tend to be larger and, contrary to Rensch's rule, dimorphism increases with species size. SSD was not related to microhabitat use. However, SSD was positively correlated with fecundity, mediated by a greater increase in female size. SSD was also influenced by parental care, suggesting that male care promotes larger male size and reduces the female bias in SSD. As suggested for other anurans, female-biased SSD in Caribbean Eleutherodactylus results from fecundity selection, although the magnitude is countered by increased male size in species with paternal care. Our results highlight the importance of considering various selective forces that may act in concert to influence the evolution of SSD.

Thermal adaptation of pelage in desert rodents balances cooling and insulation

Eric A. Riddell, James L. Patton, Steven R. Beissinger — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Phenotypic convergence across distantly related taxa can be driven by similar selective pressures from the environment or intrinsic constraints. The roles of these processes on physiological strategies, such as homeothermy, are poorly understood. We studied the evolution of thermal properties of mammalian pelage in a diverse community of rodents inhabiting the Mojave Desert, USA. We used a heat flux device to measure the thermal insulation of museum specimens and determined whether thermal properties were associated with habitat preferences while assessing phylogenetic dependence. Species that prefer arid habitats exhibited lower conductivity and thinner pelage relative to species with other habitat preferences. Despite being thinner, the pelage of arid species exhibited comparable insulation to the pelage of the other species due to its lower conductivity. Thus, arid species have insulative pelage while simultaneously benefitting from thin pelage that promotes convective cooling. We found no evidence of intrinsic constraints or phylogenetic dependence, indicating pelage readily evolves to environmental pressures. Thermoregulatory simulations demonstrated that arid specialists reduced energetic costs required for homeothermy by 14.5% by evolving lower conductivity, providing support for adaptive evolution of pelage. Our study indicates that selection for lower energetic requirements of homeothermy has shaped evolution of pelage thermal properties.

The effect of experimental hybridization on cognition and brain anatomy: Limited phenotypic variation and transgression in Poeciliidae

Catarina Vila‐Pouca, Hannah De Waele, Alexander Kotrschal — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Hybridization can promote phenotypic variation and often produces trait combinations distinct from the parental species. This increase in available variation can lead to the manifestation of functional novelty when new phenotypes bear adaptive value under the environmental conditions in which they occur. Although the role of hybridization as a driver of variation and novelty in traits linked to fitness is well recognized, it remains largely unknown whether hybridization can fuel behavioral novelty by promoting phenotypic variation in brain morphology and/or cognitive traits. To address this question, we investigated the effect of hybridization on brain anatomy, learning ability, and cognitive flexibility in first- and second-generation hybrids of two closely related fish species (Poecilia reticulata and Poecilia wingei). Overall, we found that F1 and F2 hybrids showed intermediate brain morphology and cognitive traits compared to parental groups. Moreover, as phenotypic dispersion and transgression were low for both brain and cognitive traits, we suggest that hybridization is not a strong driver of brain anatomical and cognitive diversification in these Poeciliidae. To determine the generality of this conclusion, hybridization experiments with cognitive tests need to be repeated in other families.

A common mechanism drives the alignment between the micro‐ and macroevolution of primate molars

Thu, 15 Dec 2022 22:42:17 -0800

Abstract

A central challenge for biology is to reveal how different levels of biological variation interact and shape diversity. However, recent experimental studies have indicated that prevailing models of evolution cannot readily explain the link between micro- and macroevolution at deep timescales. Here, we suggest that this paradox could be the result of a common mechanism driving a correlated pattern of evolution. We examine the proportionality between genetic variance and patterns of trait evolution in a system whose developmental processes are well understood to gain insight into how such alignment between morphological divergence and genetic variation might be maintained over macroevolutionary time. Primate molars present a model system by which to link developmental processes to evolutionary dynamics because of the biased pattern of variation that results from the developmental architecture regulating their formation. We consider how this biased variation is expressed at the population level, and how it manifests through evolution across primates. There is a strong correspondence between the macroevolutionary rates of primate molar divergence and their genetic variation. This suggests a model of evolution in which selection is closely aligned with the direction of genetic variance, phenotypic variance, and the underlying developmental architecture of anatomical traits.

Digest: Detecting genomic adaptation to sexual selection at scale using available data

Scott William Roy — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

The availability of genome sequences from large numbers of species offers the prospect of studying genotype-phenotype correlations across various phylogenetic scales using only available data. A new study illustrates the power of this approach, showing an association across primates between morphological sexual dimorphism and the prevalence of a class of DNA elements that stimulate gene expression in response to male androgens.

Digest: Evolution of plasticity and its potential role in the decline of specialists

Sharon Zhou, Laura E. Hunter — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

How does plasticity evolve over relatively short timescales? Through a series of common garden and reciprocal transplant experiments, Walter et al. found distinct patterns of variation in the phenotype and gene expression for two closely related Sicilian daisy species of the genus Senecio across an elevational gradient. This suggests that adaptive divergence may produce interspecific differences in both the magnitude and direction of plasticity. The nonadaptive nature of the plasticity found in Senecio aethnensis has important implications for conservation efforts and evolutionary modeling.

Issue information ‐ Ed Board

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 2791-2793, December 2022.

Retracted: Tyler Larsen, Cara Jefferson, Anthony Bartley, Joan E. Strassmann, David C. Queller, Inference of symbiotic adaptations in nature using experimental evolution. Evolution 2021, 75(4), 945–955 (https://doi.org/10.1111/evo.14193)

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 3073-3073, December 2022.

Correction to “Evolutionary consequences of pesticide exposure include transgenerational plasticity and potential terminal investment transgenerational effects”

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 3078-3078, December 2022.

Erratum to “Paternal genome elimination promotes altruism in viscous populations”

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 3077-3077, December 2022.

Erratum to “Elevational divergence in pigmentation plasticity is associated with selection and pigment biochemistry”

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 3075-3076, December 2022.

Correction for Kulbaba et al. (2019)

Thu, 15 Dec 2022 22:42:17 -0800

Evolution, Volume 76, Issue 12, Page 3074-3074, December 2022.

Mating strategy predicts gene presence/absence patterns in a genus of simultaneously hermaphroditic flatworms

R. Axel W. Wiberg, Gudrun Viktorin, Lukas Schärer — Thu, 15 Dec 2022 22:42:17 -0800

Abstract

Gene repertoire turnover is a characteristic of genome evolution. However, we lack well-replicated analyses of presence/absence patterns associated with different selection contexts. Here, we study ∼100 transcriptome assemblies across Macrostomum, a genus of simultaneously hermaphroditic flatworms exhibiting multiple convergent shifts in mating strategy and associated reproductive morphologies. Many species mate reciprocally, with partners donating and receiving sperm at the same time. Other species convergently evolved to mate by hypodermic injection of sperm into the partner. We find that for orthologous transcripts annotated as expressed in the body region containing the testes, sequences from hypodermically inseminating species diverge more rapidly from the model species, Macrostomum lignano, and have a lower probability of being observed in other species. For other annotation categories, simpler models with a constant rate of similarity decay with increasing genetic distance from M. lignano match the observed patterns well. Thus, faster rates of sequence evolution for hypodermically inseminating species in testis-region genes result in higher rates of homology detection failure, yielding a signal of rapid evolution in sequence presence/absence patterns. Our results highlight the utility of considering appropriate null models for unobserved genes, as well as associating patterns of gene presence/absence with replicated evolutionary events in a phylogenetic context.

Corrigendum

Thu, 14 Sep 2017 00:00:00 -0700

Evolution, EarlyView.

Erratum

Fri, 17 Jul 2015 00:00:00 -0700

Evolution, EarlyView.