Joshua trees are long-lived perennial monocots native to the Mojave Desert in North America. Composed of two species, Yucca brevifolia and Y. jaegeriana (Asparagaceae), Joshua trees are imperiled by climate change, with decreases in suitable habitat predicted under future climate change scenarios. Relatively little is understood about the ecophysiology of Joshua trees across their range, including the extent to which populations are locally adapted or phenotypically plastic to environmental stress. Plants in our common gardens showed evidence of Crassulacean acid metabolism photosynthesis (CAM) in a pilot experiment, despite no prior report of this photosynthetic pathway in these species. We further studied the variation and strength of CAM within a single common garden, measuring seedlings representing populations across the range of the two species. A combination of physiology and transcriptomic data showed low levels of CAM that varied across populations but were unrelated to home environmental conditions. Gene expression confirmed CAM activity and further suggested differences in carbon and nitrogen metabolism between Y. brevifolia and Y. jaegeriana. Together the results suggest greater physiological diversity between these species than initially expected, particularly at the seedling stage, with implications for future survival of Joshua trees under a warming climate.

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.

Yucca moths (Tegeticula and Parategeticula) are specialized pollinators of yucca plants, possessing unique, tentacle-like mouthparts used to actively collect pollen and deposit it onto the flowers of their hosts. The moths' larvae feed on the developing seeds and fruit tissue. First described in 1873, the yucca-yucca moth pollination system is now considered the archetypical example of a coevolved intimate mutualism. Research conducted over the past three decades has transformed our understanding of yucca moth diversity and host plant interactions. We summarize the current understanding of the diversity, ecology, and evolution of this group, review evidence for coevolution of the insects and their hosts, and describe how the nature of the interaction varies across evolutionary time and ecological contexts. Finally, we identify unresolved questions and areas for future research.

The Mojave Desert contains the hottest, driest regions in North America and is also one of the most ecologically intact regions in the contiguous United States. However, a confluence of factors including urbanization, climate change, and energy development are rapidly transforming this ecoregion. As a result of these growing threats, even common, widespread Mojave Desert endemics are at risk of being driven to extinction by the end of the 21st century. Ironically, renewable energy development that could delay or even reverse the effects of climate change in the region is also a potentially significant source of habitat loss for these same organisms. Protecting the Mojave therefore presents difficult choices about how to select among different conservation priorities. We argue that these choices will necessarily involve compromises in which protections for some habitats will have to be prioritized while allowing development in other areas. We review the state of conservation in the Mojave and use the Mojave Desert's iconic Joshua trees (Yucca brevifolia and Y. jaegeriana) as a case study to describe a framework for identifying habitats that should be given the highest levels of protection to ensure climate change resilience. Finally, using existing spatial data, we evaluate land use and conservation status in the Mojave. The result identifies considerable scope for compromise between conservation and renewable energy development. Although our examples are specific to the Mojave, we argue that these recommendations apply broadly to many biological communities threatened by climate change.

IntroductionForecasting range shifts in response to climate change requires accurate species distribution models (SDMs), particularly at the margins of species' ranges. However, most studies producing SDMs rely on sparse species occurrence datasets from herbarium records and public databases, along with random pseudoabsences. While environmental covariates used to fit SDMS are increasingly precise due to satellite data, the availability of species occurrence records is still a large source of bias in model predictions. We developed distribution models for hybridizing sister species of western and eastern Joshua trees (Yucca brevifolia and Y. jaegeriana, respectively), iconic Mojave Desert species that are threatened by climate change and habitat loss.MethodsWe conducted an intensive visual grid search of online satellite imagery for 672,043 0.25 km2 grid cells to identify the two species' presences and absences on the landscape with exceptional resolution, and field validated 29,050 cells in 15,001 km of driving. We used the resulting presence/absence data to train SDMs for each Joshua tree species, revealing the contemporary environmental gradients (during the past 40 years) with greatest influence on the current distribution of adult trees.ResultsWhile the environments occupied by Y. brevifolia and Y. jaegeriana were similar in total aridity, they differed with respect to seasonal precipitation and temperature ranges, suggesting the two species may have differing responses to climate change. Moreover, the species showed differing potential to occupy each other's geographic ranges: modeled potential habitat for Y. jaegeriana extends throughout the range of Y. brevifolia, while potential habitat for Y. brevifolia is not well represented within the range of Y. jaegeriana.DiscussionBy reproducing the current range of the Joshua trees with high fidelity, our dataset can serve as a baseline for future research, monitoring, and management of this species, including an increased understanding of dynamics at the trailing and leading margins of the species' ranges and potential for climate refugia.

Biological Sciences and Swire Institute of Marine Science, The University of Hong Kong, Hong Kong, Hong Kong SAR, China, 3 School of Plant Sciences, University of Arizona, Tucson, AZ, United States, Department of Life and Environmental Sciences, University of California, Merced, Merced, CA, United States, 5 Integrative Marine Ecology Department, Stazione Zoologica Anton Dohrn National Institute of Marine Biology, Ecology and Biotechnology, Naples, Italy, Department of Biosciences, Rice University, Houston, TX, United States, 7 School of Biological Sciences, University of Queensland, Brisbane, QLD, Australia, Department of Zoology, Institute of Zoology, University of Wuppertal, Wuppertal, Germany, Division of Invertebrate Zoology and Sackler Institute for Comparative Genomics, American Museum of Natural History, New York, NY, United States, Department of Ecology and Evolutionary Biology, University of Colorado Boulder, Boulder, CO, United States, Department of Biology, University of Copenhagen, Copenhagen, Denmark, 12 School of Life and Environmental Sciences, The University of Sydney, Sydney, NSW, Australia, Department of Molecular and Cell Biology, University of California, Merced, Merced, CA, United States, Department of Biological Sciences, University of Rhode Island, Kingstown, RI, United States, Department of Plant and Microbial Biology, University of California, Berkeley, Berkeley, CA, United States, Marine Ecology and Biodiversity, Plymouth Marine Laboratory, Plymouth, United Kingdom, Department of Biology, Willamette University, Salem, OR, United States, Department of Biochemistry, Microbiology and Immunology, Wayne State University School of Medicine, Detroit, MI, United States, Division of Biological Sciences, School of Science

PREMISE:Joshua trees (Yucca brevifolia and Y. jaegeriana) and their yucca moth pollinators (Tegeticula synthetica and T. antithetica) are a model system for studies of plant-pollinator coevolution and, they are thought to be one of the only cases in which there is compelling evidence for cospeciation driven by coevolution. Previous work attempted to evaluate whether divergence between the plant and their pollinators was contemporaneous. That work concluded that the trees diverged more than 5 million years ago-well before the pollinators. However, clear inferences were hampered by a lack of data from the nuclear genome and low genetic variation in chloroplast genes. As a result, divergence times in the trees could not be confidently estimated.METHODS:We present an analysis of whole chloroplast genome sequence data and RADseq data from >5000 loci in the nuclear genome. We developed a molecular clock for the Asparagales and the Agavoideae using multiple fossil calibration points. Using Bayesian inference, we produced new estimates for the age of the genus Yucca and for Joshua trees. We used calculated summary statistics describing genetic variation and used coalescent-based methods to estimate population genetic parameters.RESULTS:We find that the Joshua trees are moderately genetically differentiated, but that they diverged quite recently (~100-200 kya), and much more recently than their pollinators.CONCLUSIONS:The results argue against the notion that coevolution directly contributed to speciation in this system, suggesting instead that coevolution with pollinators may have reinforced reproductive isolation following initial divergence in allopatry.

Coevolution frequently plays an important role in diversification, but the role of obligate pollination mutualisms in the maintenance of hybrid zones has rarely been investigated. Like most members of the genus Yucca, the two species of Joshua tree (Yucca brevifolia and Yucca jaegeriana) are involved in a tightly coevolved mutualism with yucca moths. There is strong evidence of a history of coevolution between Joshua trees and their moth pollinators. We use a geographic clines approach in the Joshua tree hybrid zone to ask if selection by the moths may currently contribute to maintaining separation between these species. We compare genomic, phenotypic, and pollinator frequency clines to test whether pollinators maintain the hybrid zone or follow it as passive participants. The results reveal dramatic overlapping genomic and pollinator clines, consistent with a narrow hybrid zone maintained by strong selection. Wider phenotypic clines and a chloroplast genomic cline displaced opposite the expected direction suggest that pollinators are not the main source of selection maintaining the hybrid zone. Rather, it seems that high levels of reproductive isolation, likely acting through multiple barriers and involving many parts of the genome, keep the hybrid zone narrow.

Yucca moths (Tegeticula spp.) are the exclusive pollinators of Joshua trees (Yucca brevifolia s. l.). The moths actively pollinate the Joshua tree flowers and lay their eggs in the style. Recent studies have revealed that the plants commonly known as Joshua trees include two distinct, sister-species of plant: Yucca brevifolia Engelm. and Yucca jaegeriana McKelvey, each pollinated by two sister-species of yucca moth Tegeticula synthetica Riley and Tegeticula antithetica Pellmyr, respectively. A number of studies have argued that the moths have coevolved with their hosts, producing a pattern of phenotype matching between moth ovipositor length and floral style length. However, the only known descriptions of yucca moth pollination and oviposition behavior on Joshua trees are observations of T. synthetica made in 1893. The behavior of T. antithetica has never been observed before. We produced the first video recordings of the behavior of T. antithetica, and measured the points of oviposition and egg placement within the floral style. We found a number of differences between the behaviors of T. antithetica and T. synthetica, which appear to be a consequence of differences in floral morphology between Y. jaegeriana and Y. brevifolia. We also found that variation in floral style length strongly influences the placement of eggs within the flower, which may explain patterns of phenotype matching described previously. However, unlike in other yucca moths, we find that the mode of oviposition is unlikely to wound the floral ovules, and thus that oviposition by T. antithetica is unlikely to prompt floral abscission.

PREMISE OF THE STUDY Speciation is a complex process that can be shaped by many factors, from geographic isolation to interspecific interactions. In Joshua trees, selection from pollinators on style length has been hypothesized to contribute to the maintenance of differentiation between two hybridizing sister species. We used population genomics approaches to measure the extent of genetic differentiation between these species, test whether selection maintains differences between them, and determine whether genetic variants associated with style length show signatures of selection. METHODS Using restriction-site-associated DNA (RAD)-sequencing, we identified 9516 single nucleotide polymorphisms (SNPs) across the Joshua tree genome. We characterized the genomic composition of trees in a narrow hybrid zone and used genomic scans to search for signatures of selection acting on these SNPs. We used a genome-wide association study to identify SNPs associated with variation in phenotypic traits, including style length, and asked whether those SNPs were overrepresented among the group under selection. KEY RESULTS The two species were highly genetically differentiated (FST = 0.25), and hybrids were relatively rare in the hybrid zone. Approximately 20% of SNPs showed evidence of selection maintaining divergence. While SNPs associated with style length were overrepresented among those under selection (P << 0.0001), the same was true for SNPs associated with highly differentiated vegetative traits. CONCLUSIONS The two species of Joshua tree are clearly genetically distinct, and selection is maintaining differences between them. We found that loci associated with differentiated traits were likely to be under selection. However, many traits other than style length appeared to be under selection. Together with the dearth of intermediate hybrids, these findings reveal that these taxa are more strongly diverged than previously suspected and that selection, likely on many targets, is maintaining separation where the two species meet and hybridize.

PREMISE OF THE STUDY: The role of floral scent in facilitating reproductive isolation between closely related plants remains poorly understood. Yucca brevifolia and Yucca jaegeriana are pollinated by different moth species in allopatry, but in a narrow contact zone, pollinator-host specificity breaks down, resulting in hybridization between species. We explored the chemical basis for reproductive isolation and hybridization in these Joshua trees by characterizing the floral scent of each species in allopatry, analyzing scent profiles from trees in the contact zone, and matching these data with genotypic and phenotypic data.METHODS: We analyzed floral volatiles using gas chromatography-mass spectrometry, tested for species divergence of scent profiles and classified trees in the contact zone as hybrid or either parental species. We used floral and vegetative morphological data and genotypic data to classify trees and analyzed whether certain trait combinations were more correlated than others with respect to assignment of trees and whether frequencies of classified tree types differed depending on which data set was used.KEY RESULTS: The Joshua tree floral scent included oxygenated 8-carbon compounds not reported for other yuccas. The two species differed (P < 0.001) in scent profiles. In the contact zone, many hybrids were found, and phenotypic traits were generally weakly correlated, which may be explained by extensive gene flow between species or by exposure to different selection pressures.CONCLUSIONS: Although the two Joshua tree species produce distinct floral scent profiles, it is insufficient to prevent attraction of associated pollinators to both hosts. Instead, floral morphology may be the key trait mediating gene flow between species.

When I heard that former New York Times science writer Nick Wade had a new book coming out on the genetics of race, I immediately preordered it on Amazon. As a teacher of evolution and the biology of race, I have often longed for an accessible textbook to distill the abstract field of human population genetics into digestible mouthfuls. My hopes were bolstered by early positive reviews of A Troublesome Inheritance. James Watson called the book, “A masterful overview,” and Charles Murray concluded, “It could be the textbook for a semester's college course on human evolution.” Imagine my disappointment. The first chapter revealed that Wade's real aim was not to review the human genomics literature, but to advance a Eugenics-era genetic determinism that claims to explain everything from the rise of the West to incarceration rates among African Americans. Many others have pointed out how rickety Wade's claims are. Allen Orr noted that, “Hard evidence for Wade's thesis is nearly nonexistent,” and recently a group of 134 population geneticists—many of them the same people that Wade cites in his book—authored a letter to The New York Times disavowing his conclusions. Dismayed as I was by the book's thin defense of scientific racism, I was almost equally disappointed by how much of the science Wade got wrong. Indeed, many of his mistakes could easily have been spotted by undergraduate students in an evolutionary biology class. Needless to say, it will not be the textbook for my course. Here are a few of the reasons why. One of Wade's recurring mantras is that human evolution has been “recent, copious, and regional,” (p. 2)—the implication being that natural selection has produced major differences between human races. In support of this claim, Wade repeatedly cites the statistic, “No less than 14% of the human genome … has changed under this recent evolutionary pressure [natural selection]” (p. 2). It is here that we encounter the first of Wade's many elementary errors. That is, Wade seems not to have fully understood that the vast majority of the human genome is not composed of genes. (Only 1% of the genome is contained in exonic regions; including regulatory elements perhaps as much as 8% is functional). The “14%” statistic comes from a recent meta-analysis by Joshua Akey that reviewed genome-wide scans for selection (Akey, 2009). However, a careful reading of Wade reveals that the “14%” he is referring to is actually the fraction of genes (not the entire genome) that have been identified as showing evidence of selection in two or more studies. 14% of genes are a tiny fraction of the genome. But even this figure is probably a significant overestimate of selection's real footprint: only 2.5% of genes have been consistently identified as having experienced positive selection. Akey noted rather dismally, “There is no escaping the general conclusion that the overlap among studies is underwhelming” (Akey, 2009: 715). This brings us to a second point that any beginning population genetics student should know, which is that different evolutionary processes can produce similar population genetic patterns. That is, particular genes may show patterns consistent with selection, even if they were not themselves targets of selection. For example, genetic hitchhiking (in which regions of the genome linked to an adaptive allele are carried to high frequency along with the selected locus) can cause large sections of the genome to exhibit patterns consistent with recent selection. Many of the regions identified in Akey's meta-analysis probably fall into this category. Similarly, population growth can produce patterns similar to those expected under positive selection. As a result, genome-wide scans for selection are highly prone to false-positives. Indeed, evidence of selection acting on the MAO-A gene (Gilad et al., 2002), which Wade leans on heavily to substantiate his claims that different races have been selected for different levels of violence and aggression, is very likely to have been a false positive. The patterns suggestive of selection at this locus probably resulted from demographic factors (Przeworski, 2002), and subsequent studies have failed to find evidence of selection in MAO-A. In addition to these basic mistakes about population genetics, Wade also seems to struggle with some of the finer points of statistics. Throughout the book, Wade consistently fails to understand that “variation within” races is not the same thing as “variation among” races. A case in point: when describing the results of genome-wide scans for selection, Wade uses evidence that different genes have been under selection in different populations to argue that natural selection has promoted divergence between races. For example, a study by Benjamin Voight et al. (2006) found 206 genomic regions that showed evidence of positive selection in Yorubans, but not in Han Chinese or western Europeans. But whereas the original authors described this as evidence of population-specific adaptation, in summarizing this work Wade consistently substitutes the word “population” with the word “race,” writing, “[The authors] looked for genes under selection in the three major races … in each race, a largely different set of genes was under selection” (p. 103). Sometimes Wade's lumping of different categories is blatant, as when he discusses Dick Lewontin's classic result that 85% of genetic diversity is within populations, while 8.3% lies between populations within races, and a mere 6.3% is attributable to differences among races (Lewontin, 1972). In his critique, Wade sums together the latter two measures to get “15% between populations,” and concludes that this is actually considerable divergence, since an FST score (i.e., the measure of genetic differentiation between populations based on reductions in the frequency of heterozygotes from what would be expected if the two populations were panmictic) of 0.15—according to Sewall Wright's rules of thumb—corresponds to “moderate genetic differentiation.” There are several problems with Wade's argument. First, Lewontin's measures are not F-statistics; Lewontin measured diversity using a Shannon–Weaver Index, not heterozygosity within and between populations. Second, even if Lewontin had computed FST using a contemporary Analysis of Molecular Variance, the resulting values would not be additive. That is, one cannot estimate the overall genetic divergence between populations by simply adding together the F-statistics from comparisons among races with those based on comparisons among populations within races. Wade is quite literally mixing together the variation “within” and “among” among races to try to inflate the overall racial differences. The most egregious of Wade's errors, however, seems to be a basic misunderstanding about the nature of scientific inquiry. Most of the book is dedicated to speculative arguments about how genetic differences between populations may explain all sorts of historical events, from long-term declines in British interest rates to the failures of United States nation building in Iraq. In making these arguments, Wade leans heavily on “plausibility”; in the absence of any concrete evidence, his ideas at least sound like they could be true. In subsequent statements, such as in an opinion piece published in Time Magazine's online edition, Wade has gone even further, writing that, “the burden of proof is surely shifted” so that the onus is now on social scientists to prove that culture—not genetics—has been the primary force shaping the history of Western Civilization (Wade, 2014). Needless to say, this is not how science works. When developing a new hypothesis, we do not begin by assuming that it must be true until we are confronted overwhelming evidence to the contrary. Instead, scientists begin by assuming the null hypothesis. As evolutionary biologists, our starting assumption is that a population is in Hardy–Weinberg equilibrium (that is, there is no evolution), and when we see evidence of evolutionary change, we assume that change is the result of neutral processes (i.e., mutation and genetic drift) until we can prove otherwise. It might be tempting to believe that social inequality is the result of natural forces beyond our control, rather than the product of social institutions we ourselves have built. But until we find the genes for liberal democracy, prudent scientific conservatism requires that we look to the environment when trying to understand why some societies prosper and others languish in poverty. As I tell my students, if you want answers to those questions, you need to take a class in sociology. Christopher Irwin Smith Department of Biology Willamette University Salem, Oregon

In animal-pollinated plants, local adaptation to pollinator behaviour or morphology can restrict gene flow among plant populations; but gene flow may also prevent divergent adaptation. Here, we examine possible effects of gene flow on plant-pollinator trait matching in two varieties of Joshua tree (Agavaceae: Yucca brevifolia). The two varieties differ in strikingly in floral morphology, which matches differences in the morphology of their pollinators. However, this codivergence is not present at a smaller scale: within the two varieties of Joshua tree, variation in floral morphology between demes is not correlated with differences in moth morphology. We use population genetic data for Joshua tree and its pollinators to test the hypotheses that gene flow between Joshua tree populations is structured by pollinator specificity, and that gene flow within the divergent plant-pollinator associations swamps' fine-scale coadaptation. Our data show that Joshua tree populations are structured by pollinator association, but the two tree varieties are only weakly isolated - meaning that their phenotypic differences are maintained in the face of significant gene flow. Coalescent analysis of gene flow between the two Joshua tree types suggests that it may be shaped by asymmetric pollinator specificity, which has been observed in a narrow zone of sympatry. Finally, we find evidence suggesting that gene flow among Joshua tree sites may shape floral morphology within one plant-pollinator association, but not the other.

Coevolution is thought to be especially important in diversification of obligate mutualistic interactions such as the one between yuccas and pollinating yucca moths. We took a three-step approach to examine if plant and pollinator speciation events were likely driven by coevolution. First, we tested whether there has been co-speciation between yuccas and pollinator yucca moths in the genus Tegeticula (Prodoxidae). Second, we tested whether co-speciation also occurred between yuccas and commensalistic yucca moths in the genus Prodoxus (Prodoxidae) in which reciprocal evolutionary change is unlikely. Finally, we examined the current range distributions of yuccas in relationship to pollinator speciation events to determine if plant and moth speciation events likely occurred in sympatry or allopatry. Co-speciation analyses of yuccas with their coexisting Tegeticula pollinator and commensalistic Prodoxus lineages demonstrated phylogenetic congruence between both groups of moths and yuccas, even though moth lineages differ in the type of interaction with yuccas. Furthermore, Yucca species within a lineage occur primarily in allopatry rather than sympatry. We conclude that biogeographic factors are the overriding force in plant and pollinator moth speciation and significant phylogenetic congruence between the moth and plant lineages is likely due to shared biogeography rather than coevolution.

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.

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.