Reconstructing 120 years of climate change impacts on Joshua tree flowering.

Quantifying how global change impacts wild populations remains challenging, especially for species poorly represented by systematic datasets. Here, we infer climate change effects on masting by Joshua trees (Yucca brevifolia and Y. jaegeriana), keystone perennials of the Mojave Desert, from 15 years of crowdsourced observations. We annotated phenophase in 10,212 geo-referenced images of Joshua trees on the iNaturalist crowdsourcing platform, and used them to train machine learning models predicting flowering from annual weather records. Hindcasting to 1900 with a trained model successfully recovers flowering events in independent historical records and reveals a slightly rising frequency of conditions supporting flowering since the early 20th Century. This reflects increased variation in annual precipitation, which drives masting events in wet years-but also increasing temperatures and drought stress, which may have net negative impacts on recruitment. Our findings reaffirm the value of crowdsourcing for understanding climate change impacts on biodiversity.

Context Dependence of Local Adaptation to Abiotic and Biotic Environments: A Quantitative and Qualitative Synthesis.

Understanding how spatially variable selection shapes adaptation is an area of long-standing interest in evolutionary ecology. Recent meta-analyses have quantified the extent of local adaptation, but the relative importance of abiotic and biotic factors in driving population divergence remains poorly understood. To address this gap, we combined a quantitative meta-analysis and a qualitative metasynthesis to (1) quantify the magnitude of local adaptation to abiotic and biotic factors and (2) characterize major themes that influence the motivation and design of experiments that seek to test for local adaptation. Using local-foreign contrasts as a metric of local adaptation (or maladaptation), we found that local adaptation was greater in the presence than in the absence of a biotic interactor, especially for plants. We also found that biotic environments had stronger effects on fitness than abiotic environments when ignoring whether those environments were local versus foreign. Finally, biotic effects were stronger at low latitudes, and abiotic effects were stronger at high latitudes. Our qualitative analysis revealed that the lens through which local adaptation has been examined differs for abiotic and biotic factors. It also revealed biases in the design and implementation of experiments that make quantitative results challenging to interpret and provided directions for future research.

Zygomorphic flowers have fewer potential pollinator species.

Botanists have long identified bilaterally symmetrical (zygomorphic) flowers with more specialized pollination interactions than radially symmetrical (actinomorphic) flowers. Zygomorphic flowers facilitate more precise contact with pollinators, guide pollinator behaviour and exclude less effective pollinators. However, whether zygomorphic flowers are actually visited by a smaller subset of available pollinator species has not been broadly evaluated. We compiled 53 609 floral visitation records in 159 communities and classified the plants' floral symmetry. Globally and within individual communities, plants with zygomorphic flowers are indeed visited by fewer species. At the same time, zygomorphic flowers share a somewhat larger proportion of their visitor species with other co-occurring plants and have particularly high sharing with co-occurring plants that also have zygomorphic flowers. Visitation sub-networks for zygomorphic species also show differences that may arise from reduced visitor diversity, including greater connectance, greater web asymmetry and lower coextinction robustness of both plants and visitor species-but these changes do not necessarily translate to whole plant-visitor communities. These results provide context for widely documented associations between zygomorphy and diversification and imply that species with zygomorphic flowers may face a greater risk of extinction due to pollinator loss.

Sanctions, Partner Recognition, and Variation in Mutualism.

Mutualistic interactions can be stabilized against invasion by noncooperative individuals by putting such "cheaters" at a selective disadvantage. Selection against cheaters should eliminate genetic variation in partner quality-yet such variation is often found in natural populations. One explanation for this paradox is that mutualism outcomes are determined not only by responses to partner performance but also by partner signals. Here, we build a model of coevolution in a symbiotic mutualism, in which hosts' ability to sanction noncooperative symbionts and recognition of symbiont signals are determined by separate loci, as are symbionts' cooperation and expression of signals. In the model, variation persists without destabilizing the interaction, in part because coevolution of symbiont signals and host recognition is altered by the coevolution of sanctions and cooperation, and vice versa. Individual-based simulations incorporating population structure strongly corroborate these results. The dual systems of sanctions and partner recognition converge toward conditions similar to some economic models of mutualistic symbiosis, in which hosts offering the right incentives to potential symbionts can initiate symbiosis without screening for partner quality. These results predict that mutualists can maintain variation in recognition of partner signals or in the ability to sanction noncooperators without destabilizing mutualism, and they reinforce the notion that studies of mutualism should consider communication between partners as well as the exchange of benefits.

Effects of Gene Action, Marker Density, and Timing of Selection on the Performance of Landscape Genomic Scans of Local Adaptation.

Genomic "scans" to identify loci that contribute to local adaptation are becoming increasingly common. Many methods used for such studies have assumed that local adaptation is created by loci experiencing antagonistic pleiotropy (AP) and that the selected locus itself is assayed, and few consider how signals of selection change through time. However, most empirical data sets have marker density too low to assume that a selected locus itself is assayed, researchers seldom know when selection was first imposed, and many locally adapted loci likely experience not AP but conditional neutrality (CN). We simulated data to evaluate how these factors affect the performance of tests for genotype-environment association (GEA). We found that 3 types of regression-based analyses (linear models, mixed linear models, and latent factor mixed models) and an implementation of BayEnv all performed well, with high rates of true positives and low rates of false positives, when the selected locus experienced AP, and when the selected locus was assayed directly. However, all tests had reduced power to detect loci experiencing CN, and the probability of detecting associations was sharply reduced when physically linked rather than causative loci were sampled. AP also maintained detectable GEAs much longer than CN. Our analyses suggest that if local adaptation is often driven by loci experiencing CN, genome-scan methods will have limited capacity to find loci responsible for local adaptation.

Understanding the coevolutionary dynamics of mutualism with population genomics.

Decades of research on the evolution of mutualism has generated a wealth of possible ways whereby mutually beneficial interactions between species persist in spite of the apparent advantages to individuals that accept the benefits of mutualism without reciprocating - but identifying how any particular empirical system is stabilized against cheating remains challenging. Different hypothesized models of mutualism stability predict different forms of coevolutionary selection, and emerging high-throughput sequencing methods allow examination of the selective histories of mutualism genes and, thereby, the form of selection acting on those genes. Here, I review the evolutionary theory of mutualism stability and identify how differing models make contrasting predictions for the population genomic diversity and geographic differentiation of mutualism-related genes. As an example of the possibilities offered by genomic data, I analyze genes with roles in the symbiosis of Medicago truncatula and nitrogen-fixing rhizobial bacteria, the first classic mutualism in which extensive genomic resources have been developed for both partners. Medicago truncatula symbiosis genes, as a group, differ from the rest of the genome, but they vary in the form of selection indicated by their diversity and differentiation - some show signs of selection expected from roles in sanctioning noncooperative symbionts, while others show evidence of balancing selection expected from coevolution with symbiont signaling factors. I then assess the current state of development for similar resources in other mutualistic interactions and look ahead to identify ways in which modern sequencing technology can best inform our understanding of mutualists and mutualism.

Coevolution and the diversification of life.

Coevolution, reciprocal adaptation between two or more taxa, is commonly invoked as a primary mechanism responsible for generating much of Earth's biodiversity. This conceptually appealing hypothesis is incredibly broad in evolutionary scope, encompassing diverse patterns and processes operating over timescales ranging from microbial generations to geological eras. However, we have surprisingly little evidence that large-scale associations between coevolution and diversity reflect a causal relationship at smaller timescales, in which coevolutionary selection is directly responsible for the formation of new species. In this synthesis, we critically evaluate evidence for the often-invoked hypothesis that coevolution is an important process promoting biological diversification. We conclude that the lack of widespread evidence for coevolutionary diversification may be best explained by the fact that coevolution's importance in diversification varies depending on the type of interaction and the scale of the diversification under consideration.

Phylogenetic signal variation in the genomes of Medicago (Fabaceae).

Genome-scale data offer the opportunity to clarify phylogenetic relationships that are difficult to resolve with few loci, but they can also identify genomic regions with evolutionary history distinct from that of the species history. We collected whole-genome sequence data from 29 taxa in the legume genus Medicago, then aligned these sequences to the Medicago truncatula reference genome to confidently identify 87 596 variable homologous sites. We used this data set to estimate phylogenetic relationships among Medicago species, to investigate the number of sites needed to provide robust phylogenetic estimates and to identify specific genomic regions supporting topologies in conflict with the genome-wide phylogeny. Our full genomic data set resolves relationships within the genus that were previously intractable. Subsampling the data reveals considerable variation in phylogenetic signal and power in smaller subsets of the data. Even when sampling 5000 sites, no random sample of the data supports a topology identical to that of the genome-wide phylogeny. Phylogenetic relationships estimated from 500-site sliding windows revealed genome regions supporting several alternative species relationships among recently diverged taxa, consistent with the expected effects of deep coalescence or introgression in the recent history of Medicago.

Asymmetric hybridization and gene flow between Joshua trees (Agavaceae: Yucca) reflect differences in pollinator host specificity.

The angiosperms are by far the largest group of terrestrial plants. Their spectacular diversity is often attributed to specialized pollination. Obligate pollination mutualisms where both a plant and its pollinator are dependent upon one another for reproduction are thought to be prone to rapid diversification through co-evolution and pollinator isolation. However, few studies have evaluated the degree to which pollinators actually mediate reproductive isolation in these systems. Here, we examine evidence for hybridization and gene flow between two subspecies of Joshua tree (Yucca brevifolia brevifolia and Yucca brevifolia jaegeriana) pollinated by two sister species of yucca moth. Previous work indicated that the pollinators differ in host specificity, and DNA sequence data suggested asymmetric introgression between the tree subspecies. Through intensive sampling in a zone of sympatry, a large number of morphologically intermediate trees were identified. These included trees with floral characters typical of Y. b. jaegeriana, but vegetative features typical of Y. b. brevifolia. The opposite combination-Y. b. brevifolia flowers with Y. b. jaegeriana vegetative morphology-never occurred. Microsatellite genotyping revealed a high frequency of genetically admixed, hybrid trees. Coalescent-based estimates of migration indicated significant gene flow between the subspecies and that the direction of gene flow matches differences in pollinator host fidelity. The data suggest that pollinator behaviour determines the magnitude and direction of gene flow between the two subspecies, but that specialized pollination alone is not sufficient to maintain species boundaries. Natural selection may be required to maintain phenotypic differences in the face of ongoing gene flow.

Nondisclosure of queer identities is associated with reduced scholarly publication rates.

Nondisclosure of lesbian, gay, bisexual, transgender, asexual, or otherwise queer (LGBTQA) identities in the workplace is both common and stressful to those who do not disclose. However, we lack direct evidence that nondisclosure of LGBTQA identity affects worker productivity. In two surveys of LGBTQA-identified scientists, we found that those who did not disclose LGBTQA identities in professional settings authored fewer peer-reviewed publications-a concrete productivity cost. In the second survey, which included straight and cisgender participants as a comparison group, we found that LGBTQA participants who disclosed their sexual orientation had publication counts more like non-LGBTQA participants than those who did not disclose, and that all three groups had similar time since first publication given their academic career stage. These results are most consistent with a productivity cost to nondisclosure of LGBTQA identity in professional settings, and suggest a concrete need to improve scientific workplace climates for sexual and gender minorities.

Plant-associate interactions and diversification across trophic levels.

Interactions between species are widely understood to have promoted the diversification of life on Earth, but how interactions spur the formation of new species remains unclear. Interacting species often become locally adapted to each other, but they may also be subject to shared dispersal limitations and environmental conditions. Moreover, theory predicts that different kinds of interactions have different effects on diversification. To better understand how species interactions promote diversification, we compiled population genetic studies of host plants and intimately associated herbivores, parasites, and mutualists. We used Bayesian multiple regressions and the BEDASSLE modeling framework to test whether host and associate population structures were correlated over and above the potentially confounding effects of geography and shared environmental variation. We found that associates' population structure often paralleled their hosts' population structure, and that this effect is robust to accounting for geographic distance and climate. Associate genetic structure was significantly explained by plant genetic structure somewhat more often in antagonistic interactions than in mutualistic ones. This aligns with a key prediction of coevolutionary theory that antagonistic interactions promote diversity through local adaptation of antagonists to hosts, while mutualistic interactions more often promote diversity via the effect of hosts' geographic distribution on mutualists' dispersal.

Characterization of microsatellite loci in Yucca brevifolia (Agavaceae) and cross-amplification in related species.

PREMISE OF THE STUDY: Microsatellite primers were characterized in Yucca brevifolia for use in population genetic studies and, particularly, analyses of gene flow between varieties. METHODS AND RESULTS: We characterized 12 microsatellite loci polymorphic in Yucca brevifolia by screening primers that were developed using an SSR-enriched library or which were previously described in Yucca filamentosa. Genetic analysis of four populations resulted in the mean number of alleles per locus ranging from 10.25 to 14.58 and mean expected heterozygosity from 0.78 to 0.88. Cross-amplification of all 12 loci was attempted in six additional yucca species. CONCLUSIONS: These loci should prove useful for population genetic research in Yucca brevifolia, and cross-amplification of these loci in related species suggests that they may be useful in studies of hybridization and introgression between species.

When does coevolution promote diversification?

Coevolutionary interactions between species are thought to be an important cause of evolutionary diversification. Despite this general belief, little theoretical basis exists for distinguishing between the types of interactions that promote diversification and those types that have no effect or that even restrict it. Using analytical models and simulations of phenotypic evolution across a metapopulation, we show that coevolutionary interactions promote diversification when they impose a cost of phenotype matching, as is the case for competition or host-parasite antagonism. In contrast, classical coevolutionary arms races have no tendency to promote or inhibit diversification, and mutualistic interactions actually restrict diversification. Together with the results of recent phylogenetic and ecological studies, these results suggest that the causes of diversification in many coevolutionary systems may require reassessment.

A Model of Queer STEM Identity in the Workplace.

Science, technology, engineering, and mathematics (STEM) fields are often stereotyped as spaces in which personal identity is subsumed in the pursuit of a single-minded focus on objective scientific truths, and correspondingly rigid expectations of gender and sexuality are widespread. This paper describes findings from a grounded theory inquiry of how queer individuals working in STEM fields develop and navigate personal and professional identities. Through our analysis, we identified three distinct but related processes of Defining a queer gender and/or sexual identity, Forming an identity as a STEM professional, and Navigating identities at work. We found that heteronormative assumptions frequently silence conversations about gender and sexuality in STEM workplaces and result in complicated negotiations of self for queer professionals. This analysis of the personal accounts of queer students, faculty, and staff in STEM reveals unique processes of identity negotiation and elucidates how different social positioning creates challenges and opportunities for inclusivity.

Evaluating genomic data for management of local adaptation in a changing climate: A lodgepole pine case study.

We evaluate genomic data, relative to phenotypic and climatic data, as a basis for assisted gene flow and genetic conservation. Using a seedling common garden trial of 281 lodgepole pine (Pinus contorta) populations from across western Canada, we compare genomic data to phenotypic and climatic data to assess their effectiveness in characterizing the climatic drivers and spatial scale of local adaptation in this species. We find that phenotype-associated loci are equivalent or slightly superior to climate data for describing local adaptation in seedling traits, but that climate data are superior to genomic data that have not been selected for phenotypic associations. We also find agreement between the climate variables associated with genomic variation and with 20-year heights from a long-term provenance trial, suggesting that genomic data may be a viable option for identifying climatic drivers of local adaptation where phenotypic data are unavailable. Genetic clines associated with the experimental traits occur at broad spatial scales, suggesting that standing variation of adaptive alleles for this and similar species does not require management at scales finer than those indicated by phenotypic data. This study demonstrates that genomic data are most useful when paired with phenotypic data, but can also fill some of the traditional roles of phenotypic data in management of species for which phenotypic trials are not feasible.

Divergence in an obligate mutualism is not explained by divergent climatic factors.

Adaptation to divergent environments creates and maintains biological diversity, but we know little about the importance of different agents of ecological divergence. Coevolution in obligate mutualisms has been hypothesized to drive divergence, but this contention has rarely been tested against alternative ecological explanations. Here, we use a well-established example of coevolution in an obligate pollination mutualism, Yucca brevifolia and its two pollinating yucca moths, to test the hypothesis that divergence in this system is the result of mutualists adapting to different abiotic environments as opposed to coevolution between mutualists. We used a combination of principal component analyses and ecological niche modeling to determine whether varieties of Y. brevifolia associated with different pollinators specialize on different environments. Yucca brevifolia occupies a diverse range of climates. When the two varieties can disperse to similar environments, they occupy similar habitats. This suggests that the two varieties have not specialized on distinct habitats. In turn, this suggests that nonclimatic factors, such as the biotic interaction between Y. brevifolia and its pollinators, are responsible for evolutionary divergence in this system.

Host specificity and reproductive success of yucca moths (Tegeticula spp. Lepidoptera: Prodoxidae) mirror patterns of gene flow between host plant varieties of the Joshua tree (Yucca brevifolia: Agavaceae).

Coevolution between flowering plants and their pollinators is thought to have generated much of the diversity of life on Earth, but the population processes that may have produced these macroevolutionary patterns remain unclear. Mathematical models of coevolution in obligate pollination mutualisms suggest that phenotype matching between plants and their pollinators can generate reproductive isolation. Here, we test this hypothesis using a natural experiment that examines the role of natural selection on phenotype matching between yuccas and yucca moths (Tegeticula spp.) in mediating reproductive isolation between two varieties of Joshua tree (Yucca brevifolia var. brevifolia and Y. brevifolia var. jaegeriana). Using passive monitoring techniques, DNA barcoding, microsatellite DNA genotyping, and sibship reconstruction, we track host specificity and the fitness consequences of host choice in a zone of sympatry. We show that the two moth species differ in their degree of host specificity and that oviposition on a foreign host plant results in the production of fewer offspring. This difference in host specificity between the two moth species mirrors patterns of chloroplast introgression from west to east between host varieties, suggesting that natural selection acting on pollinator phenotypes mediates gene flow and reproductive isolation between Joshua-tree varieties.

Distinguishing coevolution from covicariance in an obligate pollination mutualism: asynchronous divergence in Joshua tree and its pollinators.

Obligate pollination mutualisms--in which both plants and their pollinators are reliant upon one another for reproduction--represent some of the most remarkable coevolutionary interactions in the natural world. The intimacy and specificity of these interactions have led to the prediction that the plants and their pollinators may be prone to cospeciation driven by coevolution. Several studies have identified patterns of phylogenetic congruence that are consistent with this prediction, but it is difficult to determine the evolutionary process that underlies these patterns. Phylogenetic congruence might also be produced by extrinsic factors, such as a shared biogeographic history. We examine the biogeographic history of a putative case of codivergence in the obligate pollination mutualism between Joshua trees (Yucca brevifolia) and two sister species of pollinating yucca moths (Tegeticula spp.) We employ molecular phylogenetic methods and coalescent-based approaches, in combination with relaxed-clock estimates of absolute rates of molecular evolution, to analyze multi-locus sequence data from more than 30 populations of Y. brevifolia and its pollinators. The results indicate that the moth species diverged significantly (p < 0.01) more recently than their corresponding host populations, suggesting that the apparent codivergence is not an artifact of a shared biogeographic history.

Coevolution and divergence in the Joshua tree/yucca moth mutualism.

Theory suggests that coevolution drives diversification in obligate pollination mutualism, but it has been difficult to disentangle the effects of coevolution from other factors. We test the hypothesis that differential selection by two sister species of pollinating yucca moths (Tegeticula spp.) drove divergence between two varieties of the Joshua tree (Yucca brevifolia) by comparing measures of differentiation in floral and vegetative features. We show that floral features associated with pollination evolved more rapidly than vegetative features extrinsic to the interaction and that a key floral feature involved in the mutualism is more differentiated than any other and matches equivalent differences in the morphology of the pollinating moths. A phylogenetically based, ancestral states reconstruction shows that differences in moth morphology arose in the time since they first became associated with Joshua trees. These results suggest that coevolution, rather than extrinsic environmental factors, has driven divergence in this obligate pollination mutualism.