Reversing extinction trends: new uses of (old) herbarium specimens to accelerate conservation action on threatened species.

Although often not collected specifically for the purposes of conservation, herbarium specimens offer sufficient information to reconstruct parameters that are needed to designate a species as 'at-risk' of extinction. While such designations should prompt quick and efficient legal action towards species recovery, such action often lags far behind and is mired in bureaucratic procedure. The increase in online digitization of natural history collections has now led to a surge in the number new studies on the uses of machine learning. These repositories of species occurrences are now equipped with advances that allow for the identification of rare species. The increase in attention devoted to estimating the scope and severity of the threats that lead to the decline of such species will increase our ability to mitigate these threats and reverse the declines, overcoming a current barrier to the recovery of many threatened plant species. Thus far, collected specimens have been used to fill gaps in systematics, range extent, and past genetic diversity. We find that they also offer material with which it is possible to foster species recovery, ecosystem restoration, and de-extinction, and these elements should be used in conjunction with machine learning and citizen science initiatives to mobilize as large a force as possible to counter current extinction trends.

Plant traits moderate pollen limitation of introduced and native plants: a phylogenetic meta-analysis of global scale.

The role of pollination in the success of invasive plants needs to be understood because invasives have substantial effects on species interactions and ecosystem functions. Previous research has shown both that reproduction of invasive plants is often pollen limited and that invasive plants can have high seed production, motivating the questions: How do invasive populations maintain reproductive success in spite of pollen limitation? What species traits moderate pollen limitation for invaders? We conducted a phylogenetic meta-analysis with 68 invasive, 50 introduced noninvasive and 1931 native plant populations, across 1249 species. We found that invasive populations with generalist pollination or pollinator dependence were less pollen limited than natives, but invasives and introduced noninvasives did not differ. Invasive species produced 3× fewer ovules/flower and >250× more flowers per plant, compared with their native relatives. While these traits were negatively correlated, consistent with a tradeoff, this did not differ with invasion status. Invasive plants that produce many flowers and have floral generalisation are able to compensate for or avoid pollen limitation, potentially helping to explain the invaders' reproductive successes.

Specialization in plant-pollinator networks: insights from local-scale interactions in Glenbow Ranch Provincial Park in Alberta, Canada.

BACKGROUND: The occurrence and frequency of plant-pollinator interactions are acknowledged to be a function of multiple factors, including the spatio-temporal distribution of species. The study of pollination specialization by examining network properties and more recently incorporating predictors of pairwise interactions is emerging as a useful framework, yet integrated datasets combining network structure, habitat disturbance, and phylogenetic information are still scarce. RESULTS: We found that plant-pollinator interactions in a grassland ecosystem in the foothills of the Rocky Mountains are not randomly distributed and that high levels of reciprocal specialization are generated by biological constraints, such as floral symmetry, pollinator size and pollinator sociality, because these traits lead to morphological or phenological mismatching between interacting species. We also detected that landscape degradation was associated with differences in the network topology, but the interaction webs still maintained a consistently higher number of reciprocal specialization cases than expected. Evidence for the reciprocal evolutionary dependence in visitors (e.g., related pollinators visiting related plants) were weak in this study system, however we identified key species joining clustered units. CONCLUSIONS: Our results indicate that the conserved links with keystone species may provide the foundation for generating local reciprocal specialization. From the general topology of the networks, plant-pollinators interactions in sites with disturbance consisted of generalized nodes connecting modules (i.e., hub and numerous connectors). Vice versa, interactions in less disturbed sites consisted of more specialized and symmetrical connections.

Y fuse? Sex chromosome fusions in fishes and reptiles.

Chromosomal fusion plays a recurring role in the evolution of adaptations and reproductive isolation among species, yet little is known of the evolutionary drivers of chromosomal fusions. Because sex chromosomes (X and Y in male heterogametic systems, Z and W in female heterogametic systems) differ in their selective, mutational, and demographic environments, those differences provide a unique opportunity to dissect the evolutionary forces that drive chromosomal fusions. We estimate the rate at which fusions between sex chromosomes and autosomes become established across the phylogenies of both fishes and squamate reptiles. Both the incidence among extant species and the establishment rate of Y-autosome fusions is much higher than for X-autosome, Z-autosome, or W-autosome fusions. Using population genetic models, we show that this pattern cannot be reconciled with many standard explanations for the spread of fusions. In particular, direct selection acting on fusions or sexually antagonistic selection cannot, on their own, account for the predominance of Y-autosome fusions. The most plausible explanation for the observed data seems to be (a) that fusions are slightly deleterious, and (b) that the mutation rate is male-biased or the reproductive sex ratio is female-biased. We identify other combinations of evolutionary forces that might in principle account for the data although they appear less likely. Our results shed light on the processes that drive structural changes throughout the genome.

Forecasting pollination declines through DNA barcoding: the potential contributions of macroecological and macroevolutionary scales of inquiry.

While pollinators are widely acknowledged as important contributors to seed production in plant communities, we do not yet have a good understanding of the importance of pollinator specialists for this ecosystem service. Determination of the prevalence of pollinator specialists is often hindered by the occurrence of cryptic species and the limitations of observational data on pollinator visitation rates, two areas where DNA barcoding of pollinators and pollen can be useful. Further, the demonstrated adequacy of pollen DNA barcoding from historical records offers opportunities to observe the effects of pollinator loss over longer timescales, and phylogenetic approaches can elucidate the historical rates of extinction of specialist lineages. In this Viewpoint article, we review how advances in DNA barcoding and metabarcoding of plants and pollinators have brought important developments to our understanding of specialization in plant-pollinator interactions. We then put forth several lines of inquiry that we feel are especially promising for providing insight on changes in plant-pollinator interactions over space and time. Obtaining estimates of the effects of reductions in specialists will contribute to forecasting the loss of ecosystem services that will accompany the erosion of plant and pollinator diversity.

Sex determination: why so many ways of doing it?

Sexual reproduction is an ancient feature of life on earth, and the familiar X and Y chromosomes in humans and other model species have led to the impression that sex determination mechanisms are old and conserved. In fact, males and females are determined by diverse mechanisms that evolve rapidly in many taxa. Yet this diversity in primary sex-determining signals is coupled with conserved molecular pathways that trigger male or female development. Conflicting selection on different parts of the genome and on the two sexes may drive many of these transitions, but few systems with rapid turnover of sex determination mechanisms have been rigorously studied. Here we survey our current understanding of how and why sex determination evolves in animals and plants and identify important gaps in our knowledge that present exciting research opportunities to characterize the evolutionary forces and molecular pathways underlying the evolution of sex determination.

Feeding the enemy: loss of nectar and nectaries to herbivores reduces tepal damage and increases pollinator attraction in Iris bulleyana.

Floral nectar usually functions as a pollinator reward, yet it may also attract herbivores. However, the effects of herbivore consumption of nectar or nectaries on pollination have rarely been tested. We investigated Iris bulleyana, an alpine plant that has showy tepals and abundant nectar, in the Hengduan Mountains of SW China. In this region, flowers are visited mainly by pollen-collecting pollinators and nectarivorous herbivores. We tested the hypothesis that, in I. bulleyana, sacrificing nectar and nectaries to herbivores protects tepals and thus enhances pollinator attraction. We compared rates of pollination and herbivory on different floral tissues in plants with flowers protected from nectar and nectary consumption with rates in unprotected control plants. We found that nectar and nectaries suffered more herbivore damage than did tepals in natural conditions. However, the amount of tepal damage was significantly greater in the flowers with protected nectaries than in the controls; this resulted in significant differences in pollinator visitation rates. These results provide the first evidence that floral nectar and nectaries may be 'sacrificed' to herbivores, leading to reduced damage to other floral tissues that are more important for reproduction.

Dioecy does not consistently accelerate or slow lineage diversification across multiple genera of angiosperms.

Dioecy, the sexual system in which male and female organs are found in separate individuals, allows greater specialization for sex-specific functions and can be advantageous under various ecological and environmental conditions. However, dioecy is rare among flowering plants. Previous studies identified contradictory trends regarding the relative diversification rates of dioecious lineages vs their nondioecious counterparts, depending on the methods and data used. We gathered detailed species-level data for dozens of genera that contain both dioecious and nondioecious species. We then applied a probabilistic approach that accounts for differential speciation, extinction, and transition rates between states to examine whether there is an association between dioecy and lineage diversification. We found a bimodal distribution, whereby dioecious lineages exhibited higher diversification in certain genera but lower diversification in others. Additional analyses did not uncover an ecological or life history trait that could explain a context-dependent effect of dioecy on diversification. Furthermore, in-depth simulations of neutral characters demonstrated that such bimodality is also found when simulating neutral characters across the observed trees. Our analyses suggest that - at least for these genera with the currently available data - dioecy neither consistently places a strong brake on diversification nor is a strong driver.

A phylogenetic study of the tribe Antirrhineae: Genome duplications and long-distance dispersals from the Old World to the New World.

PREMISE OF THE STUDY: Antirrhineae is a large tribe within Plantaginaceae. Mostly concentrated in the Mediterranean Basin, the tribe members are present both in the Old World and the New World. Current Antirrhineae phylogenies have different views on taxonomic relationships, and they lack homogeneity in terms of geographic distribution and ploidy levels. This study aims to investigate the changes in the chromosome numbers along with dispersal routes as definitive characters identifying clades. METHODS: With the use of multiple DNA regions and taxon sampling enriched with de novo sequences, we provide an extensive phylogeny for Antirrhineae. The reconstructed phylogeny was then used to investigate changes in ploidy levels and dispersal patterns in the tribe using ChromEvol and RASP, respectively. KEY RESULTS: Antirrhineae is a monophyletic group with six highly supported clades. ChromEvol analysis suggests the ancestral haploid chromosome number for the tribe is six, and that the tribe has experienced several duplications and gain events. The Mediterranean Basin was estimated to be the origin for the tribe with four long-distance dispersals from the Old World to the New World, three of which were associated with genome duplications. CONCLUSIONS: On an updated Antirrhineae phylogeny, we showed that the three out of four dispersals from the Old World to the New World were coupled with changes in ploidy levels. The observed patterns suggest that increases in ploidy levels may facilitate dispersing into new environments.

The scope of Baker's law.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.

Evolutionary ecology of specialization: insights from phylogenetic analysis.

In this Special feature, we assemble studies that illustrate phylogenetic approaches to studying salient questions regarding the effect of specialization on lineage diversification. The studies use an array of techniques involving a wide-ranging collection of biological systems (plants, butterflies, fish and amphibians are all represented). Their results reveal that macroevolutionary examination of specialization provides insight into the patterns of trade-offs in specialized systems; in particular, the genetic mechanisms of trade-offs appear to extend to very different aspects of life history in different groups. In turn, because a species may be a specialist from one perspective and a generalist in others, these trade-offs influence whether we perceive specialization to have effects on the evolutionary success of a lineage when we examine specialization only along a single axis. Finally, how geographical range influences speciation and extinction of specialist lineages remains a question offering much potential for further insight.

Traits and phylogenetic history contribute to network structure across Canadian plant-pollinator communities.

Interaction webs, or networks, define how the members of two or more trophic levels interact. However, the traits that mediate network structure have not been widely investigated. Generally, the mechanism that determines plant-pollinator partnerships is thought to involve the matching of a suite of species traits (such as abundance, phenology, morphology) between trophic levels. These traits are often unknown or hard to measure, but may reflect phylogenetic history. We asked whether morphological traits or phylogenetic history were more important in mediating network structure in mutualistic plant-pollinator interaction networks from Western Canada. At the plant species level, sexual system, growth form, and flower symmetry were the most important traits. For example species with radially symmetrical flowers had more connections within their modules (a subset of species that interact more among one another than outside of the module) than species with bilaterally symmetrical flowers. At the pollinator species level, social species had more connections within and among modules. In addition, larger pollinators tended to be more specialized. As traits mediate interactions and have a phylogenetic signal, we found that phylogenetically close species tend to interact with a similar set of species. At the network level, patterns were weak, but we found increasing functional trait and phylogenetic diversity of plants associated with increased weighted nestedness. These results provide evidence that both specific traits and phylogenetic history can contribute to the nature of mutualistic interactions within networks, but they explain less variation between networks.

Macroevolution of the plant-hummingbird pollination system.

Plant-hummingbird interactions are considered a classic example of coevolution, a process in which mutually dependent species influence each other's evolution. Plants depend on hummingbirds for pollination, whereas hummingbirds rely on nectar for food. As a step towards understanding coevolution, this review focuses on the macroevolutionary consequences of plant-hummingbird interactions, a relatively underexplored area in the current literature. We synthesize prior studies, illustrating the origins and dynamics of hummingbird pollination across different angiosperm clades previously pollinated by insects (mostly bees), bats, and passerine birds. In some cases, the crown age of hummingbirds pre-dates the plants they pollinate. In other cases, plant groups transitioned to hummingbird pollination early in the establishment of this bird group in the Americas, with the build-up of both diversities coinciding temporally, and hence suggesting co-diversification. Determining what triggers shifts to and away from hummingbird pollination remains a major open challenge. The impact of hummingbirds on plant diversification is complex, with many tropical plant lineages experiencing increased diversification after acquiring flowers that attract hummingbirds, and others experiencing no change or even a decrease in diversification rates. This mixed evidence suggests that other extrinsic or intrinsic factors, such as local climate and isolation, are important covariables driving the diversification of plants adapted to hummingbird pollination. To guide future studies, we discuss the mechanisms and contexts under which hummingbirds, as a clade and as individual species (e.g. traits, foraging behaviour, degree of specialization), could influence plant evolution. We conclude by commenting on how macroevolutionary signals of the mutualism could relate to coevolution, highlighting the unbalanced focus on the plant side of the interaction, and advocating for the use of species-level interaction data in macroevolutionary studies.

Factors influencing diversification in angiosperms: at the crossroads of intrinsic and extrinsic traits.

Recent studies indicate that both key innovations and available area influence species richness in angiosperms. Available area has been observed to have the greatest effect, however, and appears to alter the "carrying capacity" of a lineage rather than alter diversification rates. Here, we review and weigh the evidence of predictors of angiosperm diversification and further dissect how area can place ecological limits on diversification of angiosperms, specifically addressing the following: (1) theoretical mechanisms by which particular intrinsic and extrinsic traits may affect diversification in angiosperm families; (2) evidence that the amount of available area determines the ecological limits on lineages; and (3) geographical distribution of diversification hotspots in angiosperms, concentrating on the effects of zygomorphy, noncontiguous area, and latitude. While we found that dispersal to numerous noncontiguous areas is most important in spurring diversification, diversification of tropical and zygomorphic families appears to be elevated by the generation of more species per given area.

Rapid isolation and cross-amplification of microsatellite markers in Plectritis congesta (Valerianaceae) with 454 sequencing.

PREMISE OF THE STUDY: Microsatellite markers were isolated and characterized in Plectritis congesta for studying the evolution of this highly variable species. METHODS AND RESULTS: We used 454 sequencing of DNA enriched for microsatellite repeats to develop microsatellite markers. This produced 262079 reads with an average length of 324 bp, representing approximately 800 microsatellite regions from which 48 primers were tested. Eleven markers reliably amplified without optimization. These primer pairs showed a high degree of heterozygosity and allelic diversity. Unexpectedly, half of the markers contained multiple peaks, with up to four alleles per individual, which suggests that either polyploidy or isolated gene duplication has occurred within this clade. These primers successfully cross-amplified in P. macrocera, indicating the utility of these markers for the genus. CONCLUSIONS: With variation in mating system and habitat, a mix of duplicated and nonduplicated markers, and high genetic variance, Plectritis is an ideal candidate model genus for studying the ecological and evolutionary consequences of gene duplication.

Widespread vulnerability of flowering plant seed production to pollinator declines.

Despite evidence of pollinator declines from many regions across the globe, the threat this poses to plant populations is not clear because plants can often produce seeds without animal pollinators. Here, we quantify pollinator contribution to seed production by comparing fertility in the presence versus the absence of pollinators for a global dataset of 1174 plant species. We estimate that, without pollinators, a third of flowering plant species would produce no seeds and half would suffer an 80% or more reduction in fertility. Pollinator contribution to plant reproduction is higher in plants with tree growth form, multiple reproductive episodes, more specialized pollination systems, and tropical distributions, making these groups especially vulnerable to reduced service from pollinators. These results suggest that, without mitigating efforts, pollinator declines have the potential to reduce reproduction for most plant species, increasing the risk of population declines.

Key innovations within a geographical context in flowering plants: towards resolving Darwin's abominable mystery.

Elucidating factors associated with diversification have been attempted in lineages as diverse as birds, mammals and angiosperms, yet has met with limited success. In flowering plants, the ambiguity of associations between traits and diversification has sparked debate since Darwin's description of angiosperm diversification as an 'abominable mystery'. Recent work has found that diversification is often diversity-dependent, suggesting that species richness depends on geographical area available more than on traits or the time available to accumulate species. Here, we undertake phylogenetic generalized least squares analyses that jointly examine the effects of age, ecoregion area and four ecological traits on diversification in 409 angiosperm families. Area explained the most variation, dwarfing the effect of traits and age, suggesting that diversity-dependent diversification is controlled by ecological limits. Within the context of area, however, traits associated with biotic pollination (zygomorphy) exhibited the greatest effect, possibly through the evolution of specialization.

Floral colour versus phylogeny in structuring subalpine flowering communities.

The relative number of seeds produced by competing species can influence the community structure; yet, traits that influence seed production, such as pollinator attraction and floral colour, have received little attention in community ecology. Here, we analyse floral colour using reflectance spectra that include near-UV and examined the phylogenetic signal of floral colour. We found that coflowering species within communities tended to be more divergent in floral colour than expected by chance. However, coflowering species were not phylogenetically dispersed, in part due to our finding that floral colour is a labile trait with a weak phylogenetic signal. Furthermore, while we found that locally rare and common species exhibited equivalent floral colour distances from their coflowering neighbours, frequent species (those found in more communities) exhibited higher colour distances from their coflowering neighbours. Our findings support recent studies, which have found that (i) plant lineages exhibit frequent floral colour transitions; and (ii) traits that influence local population dynamics contribute to community structure.

Land use and pollinator dependency drives global patterns of pollen limitation in the Anthropocene.

Land use change, by disrupting the co-evolved interactions between plants and their pollinators, could be causing plant reproduction to be limited by pollen supply. Using a phylogenetically controlled meta-analysis on over 2200 experimental studies and more than 1200 wild plants, we ask if land use intensification is causing plant reproduction to be pollen limited at global scales. Here we report that plants reliant on pollinators in urban settings are more pollen limited than similarly pollinator-reliant plants in other landscapes. Plants functionally specialized on bee pollinators are more pollen limited in natural than managed vegetation, but the reverse is true for plants pollinated exclusively by a non-bee functional group or those pollinated by multiple functional groups. Plants ecologically specialized on a single pollinator taxon were extremely pollen limited across land use types. These results suggest that while urbanization intensifies pollen limitation, ecologically and functionally specialized plants are at risk of pollen limitation across land use categories.

Nonrandom extinction leads to elevated loss of angiosperm evolutionary history.

The phylogenetic clustering of extinction may jeopardize the existence of entire families and genera, which can result in elevated reductions of evolutionary history (EH), trait diversity, and ecosystem functioning. Analyses of globally threatened birds and mammals suggest current extinction threats will result in a much higher loss of EH than random extinction scenarios, while the analyses of the taxonomical distribution of regionally rare plants find the opposite pattern. The disproportionately high number of rare plant species within species-rich families potentially suggests that lower losses of plant EH will be sustained than expected under random extinction. We show that at a global scale, this is not the case. Species-poor (especially monotypic) angiosperm families are more often at risk of extinction than expected. Because these high-risk species-poor families are as evolutionarily distinct as other families, the expected family-level EH plausibly lost in the next 100 years exceeds that predicted from random extinction by up to approximately 1165 million years.