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Data from: Macroevolutionary persistence of heritable endosymbionts: acquisition, retention, and expression of adaptive phenotypes in Spiroplasma

The phylogenetic incongruence between insects and their facultative maternally transmitted endosymbionts indicates that these infections are generally short-lived evolutionarily. Therefore, long-term persistence of many endosymbionts must depend on their ability to colonize and spread within new host species. At least 17 species of Drosophila are infected with endosymbiotic Spiroplasma that have various phenotypic effects. We transinfected five strains of Spiroplasma from three divergent clades into Drosophila neotestacea to test their capacity to spread in a novel host. A strain that causes male killing in Drosophila melanogaster (its native host) also does so in D. neotestacea, even though these host species diverged 40–60 mya. A strain native to D. neotestacea (designated sNeo) and the two other strains of the poulsonii clade of Spiroplasma confer resistance to wasp parasitism, suggesting that this trait may be ancestral within this clade of Spiroplasma. Conversely, no strain other than sNeo conferred resistance to the sterilizing effects of nematode parasitism, suggesting that nematode resistance is a recently derived condition. The apparent addition of nematode resistance to a Spiroplasma lineage that already confers resistance to wasp parasitism suggests endosymbionts can increase the repertoire of traits conducive to their spread. The capacity of an endosymbiont to undergo maternal transmission and express adaptive phenotypes in novel hosts, without requiring a period of host–symbiont co-evolution, enables the spread of such symbionts immediately after the colonization of a new host. This could be critical for the macroevolutionary persistence of facultative endosymbionts whose sojourn times within individual host species are relatively brief.

Data from: Cannibalism as an interacting phenotype: pre-cannibalistic aggression is influenced by social partners in the endangered Socorro isopod (Thermosphaeroma thermophilum)

Models for the evolution of cannibalism highlight the importance of asymmetries between individuals in initiating cannibalistic attacks. Studies may include measures of body size but typically group individuals into size/age classes or compare populations. Such broad comparisons may obscure the details of interactions that ultimately determine how socially contingent characteristics evolve. We propose that understanding cannibalism is facilitated by using an interacting phenotypes perspective that includes the influences of the phenotype of a social partner on the behaviour of a focal individual and focuses on variation in individual pairwise interactions. We investigated how relative body size, a composite trait between a focal individual and its social partner, and the sex of the partners influenced precannibalistic aggression in the endangered Socorro isopod, Thermosphaeroma thermophilum. We also investigated whether differences in mating interest among males and females influenced cannibalism in mixed sex pairs. We studied these questions in three populations that differ markedly in range of body size and opportunities for interactions among individuals. We found that relative body size influences the probability of and latency to attack. We observed differences in the likelihood of and latency to attack based on both an individual's sex and the sex of its partner but found no evidence of sexual conflict. The instigation of precannibalistic aggression in these isopods is therefore a property of both an individual and its social partner. Our results suggest that interacting phenotype models would be improved by incorporating a new conditional ψ, which describes the strength of a social partner's influence on focal behaviour.

opencc-zeroDec 2015View details →

Data from: Mimicry refinement: Phenotypic variations tracking the local optimum

1. Müllerian mimicry between chemically defended preys is a textbook example of natural selection favouring phenotypic convergence onto a shared warning signal. Studies of mimicry have concentrated on deciphering the ecological and genetic underpinnings of dramatic switches in mimicry association, producing a well-known mosaic distribution of mimicry patterns across geography. However, little is known about the accuracy of resemblance between natural co-mimics when the local phenotypic optimum varies. 2. In this study, using analyses of wing shape, pattern and hue, we quantify multimodal phenotypic similarity between butterfly co-mimics sharing the so-called postman pattern in different localities with varying species composition. 3. We show that subtle but consistent variation between populations of the localised species, Heliconius timareta thelxinoe, enhance resemblance to the abundant co-mimics which drive the mimicry in each locality. 4. Those results suggest that rarer co-mimics track the changes in the phenotypic optimum caused by gradual changes in the composition of the mimicry community, providing insights into the process by which intra-specific diversity of mimetic pattern may arise. Furthermore, our results suggest a multimodal evolution of similarity, with coordinated convergence in different features of the phenotype such as wing outline, pattern and hue. 5. Finally, multilocus genotyping allows estimating local hybridization rates between H. timareta and co-mimic H. melpomene in different populations, raising the hypothesis that mimicry refinement between closely-related co-mimics may be enhanced by adaptive introgression at loci modifying the accuracy of resemblance.

Data from: Phenotypic and genetic divergence among harbour porpoise populations associated with habitat regions in the North Sea and adjacent seas.

Determining the mechanisms that generate population structure is essential to the understanding of speciation and the evolution of biodiversity. Here, we investigate a geographic range that transects two habitat gradients, the North Sea to North Atlantic transition, and the temperate to sub-polar regions. We studied the harbour porpoise (Phocoena phocoena), a small odontocete inhabiting both sub-polar and temperate waters. To assess differentiation among putative populations we measured morphological variation at cranial traits (N=462 individuals) and variation at eight microsatellite loci for 338 of the same individuals from Norwegian, British and Danish waters. Significant morphological differentiation reflected the size of the buccal cavity. Porpoises forage in relatively shallow waters preying mainly on benthic species in British and Danish waters, and on mesopelagic and pelagic fish off the coast of Norway. We suggest that the observed differentiation may be explained by resource specialization and either adaptation or developmental responses to different local habitats.

opencc-zeroDec 2016View details →

Data from: Field-based high throughput phenotyping rapidly identifies genomic regions controlling yield components in rice

To ensure food security in the face of population growth, decreasing water and land for agriculture, and increasing climate variability, crop yields must increase faster than the current rates. Increased yields will require implementing novel approaches in genetic discovery and breeding. Here we demonstrate the potential of field-based high throughput phenotyping (HTP) on a large recombinant population of rice to identify genetic variation underlying important traits. We find that detecting quantitative trait loci (QTL) with HTP phenotyping is as accurate and effective as traditional labor-intensive measures of flowering time, height, biomass, grain yield, and harvest index. Genetic mapping in this population, derived from a cross of an modern cultivar (IR64) with a landrace (Aswina), identified four alleles with negative effect on grain yield that are fixed in IR64, demonstrating the potential for HTP of large populations as a strategy for the second green revolution.

opencc-zeroJun 2019View details →

Data from: Drift versus selection as drivers of phenotypic divergence at small spatial scales: the case of Belgjarskógur threespine stickleback

Divergence in phenotypic traits is facilitated by a combination of natural selection, phenotypic plasticity, gene flow and genetic drift, whereby the role of drift is expected to be particularly important in small and isolated populations. Separating the components of phenotypic divergence is notoriously difficult, particularly for multivariate phenotypes. Here we assessed phenotypic divergence of threespine stickleback (Gasterosteus aculeatus) across 19 semi-interconnected ponds within a small geographic region (~7.5 km2) using multivariate comparisons of phenotypic divergence (PST) neutral genetic (FST) and environmental (EST) variation. We found phenotypic divergence across the ponds in a suite of functionally relevant phenotypic traits, including feeding, defense and swimming traits and body shape (geometric morphometric). Comparisons of PSTs with FSTs suggest that phenotypic divergence is predominantly driven by neutral or stabilizing selection, whereas phenotypic divergence in defensive traits is in accordance with divergent selection. Comparisons of population pairwise PSTs with ESTs suggest that phenotypic divergence in swimming traits is correlated with prey availability, whereas there were no clear associations between phenotypic divergence and environmental difference in the other phenotypic groups. Overall, our results suggest that phenotypic divergence of these small populations at small geographic scales is largely driven by neutral processes (gene flow, drift), although environmental determinants (natural selection or phenotypic plasticity) may play a role.

Data from: Ecologically diverse and distinct neighbourhoods trigger persistent phenotypic consequences, and amine metabolic profiling detects them

1.Global change triggers rapid alterations in the composition and diversity of plant communities which may change ecosystem functioning. Do changes in community diversity also change traits persistently, i.e. does coexistence with numerous or functionally or phylogenetically distinct species trigger, in a given focal species, trait shifts that persist? 2.We studied the grass Dactylis glomerata. Dactylis was grown in experimental plots with different species compositions for five years, sampled, cloned and grown in a common garden. We studied amines, regulators integrating growth responses of organisms to their environment. 3.We found that the mean levels and variances of most amines depended on the diversity of the source community, notably the species richness and the phylogenetic and functional distinctness from Dactylis, unbiased by species identity or biomass shifts. 4.Synthesis. Our results suggest that different levels of ambient diversity can, within a few years, select for different genotypes which have different compositions of growth regulators. Our study also suggests that a plant species can evolve in response to the diversity or distinctness of the surrounding plant community. Evolutionary changes of plant phenotypes might mediate an impact of past biological diversity on present ecosystem functioning.

Data from: Phenotypic plasticity and adaptive evolution contribute to advancing flowering phenology in response to climate change

Anthropogenic climate change has already altered the timing of major life history transitions, such as the initiation of reproduction. Both phenotypic plasticity and adaptive evolution can underlie rapid phenological shifts in response to climate change but their relative contributions are poorly understood. Here, we combine a continuous 38-year field survey with quantitative genetic field experiments to assess adaptation in the context of climate change. We focused on Boechera stricta (Brassicaeae), a mustard native to the U.S. Rocky Mountains. Flowering phenology advanced significantly from 1973-2011, and was strongly associated with warmer temperatures and earlier snowmelt dates. Strong directional selection favored earlier flowering in contemporary environments (2010-2011). Climate change could drive this directional selection, and promote even earlier flowering as temperatures continue to increase. Our quantitative genetic analyses predict a response to selection of 0.2 to 0.5 days acceleration in flowering per generation, which could account for more than 20% of the phenological change observed in the long-term dataset. However, the strength of directional selection and the predicted evolutionary response are likely much greater now than even 30 years ago because of rapidly changing climatic conditions. We predict that adaptation will likely be necessary for long-term in situ persistence in the context of climate change.

Data from: Sun skink landscape genomics: assessing how microevolutionary processes shape genetic and phenotypic diversity across a heterogeneous and fragmented landscape

Incorporating genomic data sets into landscape genetic analyses allows for powerful insights into population genetics, explicitly geographical correlates of selection, and morphological diversification of organisms across the geographical template. Here, we utilize an integrative approach to examine gene flow and detect selection, and we relate these processes to genetic and phenotypic population differentiation across South-East Asia in the common sun skink, Eutropis multifasciata. We quantify the relative effects of geographic and ecological isolation in this system and find elevated genetic differentiation between populations from island archipelagos compared to those on the adjacent South-East Asian continent, which is consistent with expectations concerning landscape fragmentation in island archipelagos. We also identify a pattern of isolation by distance, but find no substantial effect of ecological/environmental variables on genetic differentiation. To assess whether morphological conservatism in skinks may result from stabilizing selection on morphological traits, we perform FST–PST comparisons, but observe that results are highly dependent on the method of comparison. Taken together, this work provides novel insights into the manner by which micro-evolutionary processes may impact macro-evolutionary scale biodiversity patterns across diverse landscapes, and provide genomewide confirmation of classic predictions from biogeographical and landscape ecological theory.

opencc-zeroDec 2016View details →

Data from: Stress hormones predict a host superspreader phenotype in the West Nile virus system

Glucocorticoid stress hormones, such as corticosterone (CORT), have profound effects on the behaviour and physiology of organisms, and thus have the potential to alter host competence and the contributions of individuals to population- and community-level pathogen dynamics. For example, CORT could alter the rate of contacts among hosts, pathogens and vectors through its widespread effects on host metabolism and activity levels. CORT could also affect the intensity and duration of pathogen shedding and risk of host mortality during infection. We experimentally manipulated songbird CORT, asking how CORT affected behavioural and physiological responses to a standardized West Nile virus (WNV) challenge. Although all birds became infected after exposure to the virus, only birds with elevated CORT had viral loads at or above the infectious threshold. Moreover, though the rate of mortality was faster in birds with elevated CORT compared with controls, most hosts with elevated CORT survived past the day of peak infectiousness. CORT concentrations just prior to inoculation with WNV and anti-inflammatory cytokine concentrations following viral exposure were predictive of individual duration of infectiousness and the ability to maintain physical performance during infection (i.e. tolerance), revealing putative biomarkers of competence. Collectively, our results suggest that glucocorticoid stress hormones could directly and indirectly mediate the spread of pathogens.

opencc-zeroDec 2017View details →

Data from: Morphological novelty emerges from pre-existing phenotypic plasticity

Plasticity-first evolution (PFE) posits that novel features arise when selection refines pre-existing phenotypic plasticity into an adaptive phenotype. However, PFE is controversial because few tests have been conducted in natural populations. Here we present evidence that PFE fostered the origin of an evolutionary novelty that allowed certain amphibians to invade a new niche—a distinctive carnivore morph. We compared morphology, gene expression and growth of three species of spadefoot toad tadpoles when reared on alternative diets: Scaphiopus holbrookii, which (like most frogs) never produce carnivores; Spea multiplicata, which sometimes produce carnivores, but only through diet-induced plasticity; and Spea bombifrons, which often produce carnivores regardless of diet. Consistent with PFE, we found diet-induced plasticity—in morphology and gene expression—in Sc. holbrookii, adaptive refinement of this plasticity in Sp. multiplicata, and further refinement of the carnivore phenotype in Sp. bombifrons. Generally, phenotypic plasticity might play a significant, if underappreciated, role in evolutionary innovation.

opencc-zeroDec 2010View details →

Data from: Persistence in peripheral refugia promotes phenotypic divergence and speciation in a rainforest frog

It is well established from the fossil record and phylogeographic analyses that late Quaternary climate fluctuations led to substantial changes in species' distribution, but whether and how these fluctuations resulted in phenotypic divergence and speciation is less clear. This question can be addressed through detailed analysis of traits relevant to ecology and mating within and among intraspecific lineages that persisted in separate refugia. In a biogeographic system (the Australian Wet Tropics, AWT) with a well-established history of refugial isolation during Pleistocene glacial periods, we test whether climate-mediated changes in distribution drove genetic and phenotypic divergence in the rainforest frog, Cophixalus ornatus. We combine paleomodeling and multilocus genetics to demonstrate long-term persistence within, and isolation among, one central and two peripheral refugia. In contrast to other AWT vertebrates, the three major lineages differ in ecologically relevant morphology and in mating call, reflecting divergent selection and/or genetic drift in the peripheral isolates. Divergence in mating call, and contact zone analyses, suggest that the lineages now represent distinct species. The results show that climate shifts can promote genetic and phenotypic divergence, and potentially speciation, and direct attention towards incorporating adaptive traits into phylogeographic studies to better resolve the mechanisms of speciation.

opencc-zeroDec 2016View details →

Data from: Testing the association of phenotypes with polyploidy: An example using herbaceous and woody eudicots

Although numerous studies have surveyed the frequency with which different plant characters are associated with polyploidy, few statistical tools are available to identify the factors that potentially facilitate polyploidy. We describe a new probabilistic model, BiChroM, designed to associate the frequency of polyploidy and chromosomal change with a binary phenotypic character in a phylogeny. BiChroM provides a robust statistical framework for testing differences in rates of polyploidy associated with phenotypic characters along a phylogeny while simultaneously allowing for evolutionary transitions between character states. We used BiChroM to test whether polyploidy is more frequent in woody or herbaceous plants, based on tree with 4,711 eudicot species. Although polyploidy occurs in woody species, rates of chromosome doubling were over six times higher in herbaceous species. Rates of single chromosome increases or decreases were also far higher in herbaceous than woody species. Simulation experiments indicate that BiChroM performs well with little to no bias and relatively little variance at a wide range of tree depths when trees have at least 500 taxa. Thus, BiChroM provides a first step towards a rigorous statistical framework for assessing the traits that facilitate polyploidy.

opencc-zeroDec 2018View details →

Data from: Extended phenotypes and foraging restrictions: ant nest entrances and resource ingress in leaf-cutting ants

Several factors may restrict the acquisition of food to below the levels predicted by the optimization theory. However, how the design of structures that animals build for foraging restrict the entry of food are less known. Using scaling relationships we determined whether the design of the entrances of leaf-cutting ant nests restricts resource input into the colony. We measured nests and foraging parameters in 25 nests of Atta cephalotes in a tropical rain forest. Ant flux was reduced to up to 60% at nest entrances. The width of all entrances per nest increased at similar rates as nest size, but the width of nest entrances increased with the width of its associated trail at rates below those expected by isometry. The fact that entrance widths grow slower than trail widths suggests that the enlargement of entrance holes does not reach the dimensions needed to avoid delays when foraging rates are high and loads are big. The enlargement of nest entrances appears to be restricted by the digging effort required to enlarge nest tunnels, and by increments in the risk of inundation, predator/parasitoid attacks, and microclimate imbalances inside the nest. The design of the extended phenotypes can also restrict the ingress of food into the organisms, offering additional evidence to better understand eventual controversies between empirical data and the foraging theory.

opencc-zeroDec 2013View details →

Data from: Adaptive, convergent origins of the pygmy phenotype in African rainforest hunter-gatherers

The evolutionary history of the human pygmy phenotype (small body size), a characteristic of African and Southeast Asian rainforest hunter-gatherers, is largely unknown. Here we use a genome-wide admixture mapping analysis to identify 16 genomic regions that are significantly associated with the pygmy phenotype in the Batwa, a rainforest hunter-gatherer population from Uganda (east central Africa). The identified genomic regions have multiple attributes that provide supporting evidence of genuine association with the pygmy phenotype, including enrichments for SNPs previously associated with stature variation in Europeans and for genes with growth hormone receptor and regulation functions. To test adaptive evolutionary hypotheses, we computed the haplotype-based integrated haplotype score (iHS) statistic and the level of population differentiation (FST) between the Batwa and their agricultural neighbors, the Bakiga, for each genomic SNP. Both |iHS| and FST values were significantly higher for SNPs within the Batwa pygmy phenotype-associated regions than the remainder of the genome, a signature of polygenic adaptation. In contrast, when we expanded our analysis to include Baka rainforest hunter-gatherers from Cameroon and Gabon (west central Africa) and Nzebi and Nzime neighboring agriculturalists, we did not observe elevated |iHS| or FST values in these genomic regions. Together, these results suggest adaptive and at least partially convergent origins of the pygmy phenotype even within Africa, supporting the hypothesis that small body size confers a selective advantage for tropical rainforest hunter-gatherers but raising questions about the antiquity of this behavior.

Data from: High levels of genetic structure and striking phenotypic variability in a sexually dimorphic suckermouth catfish from the African Highveld

Uncovering biological diversity to more accurately understand diversity patterns, and ultimately the processes driving diversification, is important not only from an evolutionary perspective but also a conservation perspective. This is particularly pertinent in Africa's rivers in which overall diversity, as well as how it arose, is poorly understood in comparison with lacustrine environments. Here we investigate population divergence in the sexually dimorphic suckermouth catfish species Chiloglanis anoterus (Crass, 1960) from the African Highveld, in which we observe striking variability in exaggerated male caudal fins across its range. As this trait is likely to be indirect evidence for sexual selection by female choice, a mechanism that has been shown to increase species diversity in different taxa, we used an integrated approach to test if current diversity in this species is underestimated. Results based on phylogenetic inference, population genetics and geometric morphometrics indicate that the recognized species C. anoterus represents five distinct lineages that may be considered confirmed candidate species. We suggest that diversification in these highland catfish has been facilitated through geographical isolation in upper river catchments, and that sexual selection through female choice has probably driven variation in male caudal fin morphology. In contrast to the relatively large range size of the currently recognized species (C. anoterus), our findings highlight highly restricted ranges of the lineages identified here, indicating that these highland habitats may harbour higher levels of endemic diversity than previously thought.

Data from: Selection towards different adaptive optima drove the early diversification of locomotor phenotypes in the radiation of Neotropical geophagine cichlids

Background: Simpson envisaged a conceptual model of adaptive radiation in which lineages diversify into "adaptive zones" within a broad adaptive landscape. However only a handful of studies have actually investigated the adaptive landscape and its implication for our interpretation of the underlying mechanisms of phenotypic evolution. In fishes the evolution of locomotor phenotypes may represent an important dimension of ecomorphological diversification during an adaptive radiation given its implications for feeding and habitat use. Neotropical geophagine cichlids represent a newly identified adaptive radiation and provide a useful system for studying patterns of locomotor diversification and the implications of selective constraints on phenotypic divergence in general. Results: We use multivariate ordination models of phenotypic evolution and posterior predictive approaches to investigate the adaptive landscape and test for evidence of early diversification of locomotor phenotypes in Geophagini. The evolution of locomotor phenotypes was characterized by divergent selection towards two distinct adaptive peaks and the early divergence of modern morphological disparity. Evolutionary models and posterior predictive approaches favoured constant-rate divergent selection over decreasing rates of phenotypic evolution as the underlying process driving the early divergence of locomotor phenotypes. Conclusions: The influence of multiple adaptive peaks on the divergence of locomotor attributes in Geophagini is compatible with the expectations of an ecologically-driven adaptive radiation. This study confirms that the diversification of locomotor morphology represents an important dimension of phenotypic evolution in the geophagine adaptive radiation. It also suggests that the commonly observed early burst of phenotypic evolution during adaptive radiations is best explained by a model that incorporates divergent selection deep in the phylogeny.

Data from: Consistency and variation in phenotypic selection exerted by a community of seed predators

Phenotypic selection that is sustained over time underlies both anagenesis and cladogenesis, but the conditions that lead to such selection and what causes variation in selection are not well known. We measured the selection exerted by three species of predispersal seed predators of lodgepole pine (Pinus contorta latifolia) in the South Hills, Idaho and found that net selection on different cone and seed traits exerted by red crossbills (Loxia curvirostra) and cone borer moths (Eucosma recissoriana) over 10 years of seed crops was similar to that measured in another mountain range. We also found that the strength of selection increased as seed predation increased, which provides a mechanism for the correlation between the escalation of seed defenses and the density of seed predators. Red crossbills consume the most seeds and selection they exert accounts for much of the selection experienced by lodgepole pine, providing additional support for a coevolutionary arms race between crossbills and lodgepole pine in the South Hills. The third seed predator, hairy woodpeckers (Picoides villosus), consumed less than one-sixth as many seeds as crossbills. Across the northern Rocky Mountains, woodpecker abundance and therefore selective impact appears limited by the elevated seed defenses of lodgepole pine.

opencc-zeroDec 2018View details →

Data from: Breeding success but not mate choice is phenotype- and context-dependent in a color polymorphic raptor

Morph-specific mate choice has been proposed as one of the evolutionary mechanisms that contribute to the maintenance of variation in color polymorphic systems. Coloration usually covaries with other phenotypic traits affecting life history and thus is often used as a criterion for mate choice. Here, we assess whether mating patterns, natal dispersal, and breeding output are phenotype-dependent in the color polymorphic Eleonora's falcon. We used a long-term dataset of 946 individually ringed adult falcons that included 109 individuals monitored from birth up to recruitment into the breeding population. Overall, patterns of mate choice with regard to coloration were neither assortative nor disassortative. Natal dispersal distance was greater in females but was not associated with coloration. Breeding success was both morph-dependent and context-dependent. Although clutch size was similar in differently colored pairs, differences arose in the number of chicks that fledge. In some years, dark males raised more offspring, regardless of female color morph. Differences in the breeding tactics between male morphs could be associated with intraspecific predation and may thus contribute to the observed differences in breeding output, especially when food availability is low. This suggests that mating patterns may interact with other factors and give rise to the observed higher breeding output of dark males only under certain environmental conditions.