The phylogeny and biogeography of Hakea (Proteaceae) reveals the role of biome shifts in a continental plant radiation

The frequency of evolutionary biome shifts during diversification has important implications for our ability to explain geographic patterns of plant diversity. Recent studies present several examples of biome shifts, but whether frequencies of biome shifts closely reflect geographic proximity or environmental similarity of biomes remains poorly known. We explore this question by using phylogenomic methods to estimate the phylogeny of Hakea, a diverse Australian genus occupying a wide range of biomes. Model‐based estimation of ancestral regions indicates that Hakea began diversifying in the Mediterranean biome of southern Australia in the Middle Eocene–Early Oligocene, and dispersed repeatedly into other biomes across the continent. We infer around 47 shifts between biomes. Frequencies of shifts between pairs of biomes are usually similar to those expected from their geographic connectedness or climatic similarity, but in some cases are substantially higher or lower than expected, perhaps reflecting how readily key physiological traits can be modified to adapt lineages to new environments. The history of frequent biome‐shifting is reflected in the structure of present‐day assemblages, which tend to be more phylogenetically diverse than null‐model expectations. The case of Hakea demonstrates that the radiation of large plant clades across wide geographic areas need not be constrained by dispersal limitation or conserved adaptations to particular environments.     

Correlated evolution between climate and suites of traits along a fast–slow continuum in the radiation of Protea

Evolutionary radiations are responsible for much of Earth's diversity, yet the causes of these radiations are often elusive. Determining the relative roles of adaptation and geographic isolation in diversification is vital to understanding the causes of any radiation, and whether a radiation may be labeled as “adaptive” or not. Across many groups of plants, trait–climate relationships suggest that traits are an important indicator of how plants adapt to different climates. In particular, analyses of plant functional traits in global databases suggest that there is an “economics spectrum” along which combinations of functional traits covary along a fast–slow continuum. We examine evolutionary associations among traits and between trait and climate variables on a strongly supported phylogeny in the iconic plant genus Protea to identify correlated evolution of functional traits and the climatic‐niches that species occupy. Results indicate that trait diversification in Protea has climate associations along two axes of variation: correlated evolution of plant size with temperature and leaf investment with rainfall. Evidence suggests that traits and climatic‐niches evolve in similar ways, although some of these associations are inconsistent with global patterns on a broader phylogenetic scale. When combined with previous experimental work suggesting that trait–climate associations are adaptive in Protea, the results presented here suggest that trait diversification in this radiation is adaptive.     

Environmental niche conservatism explains the accumulation of species richness in Mediterranean‐hotspot plant genera

The causes of exceptionally high plant diversity in Mediterranean‐climate biodiversity hotspots are not fully understood. We asked whether a mechanism similar to the tropical niche conservatism hypothesis could explain the diversity of four large genera (Protea, Moraea, Banksia, and Hakea) with distributions within and adjacent to the Greater Cape Floristic Region (South Africa) or the Southwest Floristic Region (Australia). Using phylogenetic and spatial data we estimated the environmental niche of each species, and reconstructed the mode and dynamics of niche evolution, and the geographic history, of each genus. For three genera, there were strong positive relationships between the diversity of clades within a region and their inferred length of occupation of that region. Within genera, there was evidence for strong evolutionary constraint on niche axes associated with climatic seasonality and aridity, with different niche optima for hotspot and nonhotspot clades. Evolutionary transitions away from hotspots were associated with increases in niche breadth and elevated rates of niche evolution. Our results point to a process of “hotspot niche conservatism” whereby the accumulation of plant diversity in Mediterranean‐type ecosystems results from longer time for speciation, with dispersal away from hotspots limited by narrow and phylogenetically conserved environmental niches.     

Mexical plant phenology: is it similar to Mediterranean communities?

The sclerophyllous, evergreen vegetation found in Mexico under tropical climate is named 'Mexical' (MEX) and presents many traits that have been thought to converge under a Mediterranean climate. Flowering phenology is strongly similar across Mediterranean-type ecosystems (MTEs) and this paper investigates MEX plant phenology in this context. The common history of the vegetation and the differences in the climatic conditions experienced by MEX and MTE taxa provide an ideal scenario to infer the relative importance of natural selection and historical constraints in the phenological response of plants to climatic conditions. This study has involved collecting field and bibliographic data on flowering phenology of MEX communities to detect (1) similarities at the community level between MTEs and MEX, (2) similarities between Tertiary and Quaternary taxa in MTEs and MEX, and (3) similarities between congeneric taxa from MEX and MTEs (taxa sharing a common ancestor but having evolved under different climates). Flowering in MEX does not occur mainly in spring, as in MTEs, but in summer, suggesting a response that maximizes water use in the rainy season. Flowering phenology of MEX species differed from their MTE congeneric species, suggesting that even though a common ancestor is shared, environmental pressures have led to different phenological responses in MEX and MTE plants. The flowering season for species that originated in the Tertiary and Quaternary did not differ in MEX, as expected, because of climatic uniformity along the whole time line. In MTEs, flowering differences between Tertiary and Quaternary species were not congruent, suggesting that the balance between the historical constraints and the selective force of the Mediterranean climate is different among the three MTEs, and a particular explanation is needed for each. © 2002 The Linnean Society of London, Botanical Journal of the Linnean Society , 2002, 138 , 297–303.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Plant functional traits along environmental gradients in seasonally dry and fire‐prone ecosystem

Questions: How does the abundance and richness of plant assemblages with different functional (regeneration and nutrient acquisition) traits vary with fire regime, moisture availability and substrate fertility? What is the role of different functional traits in maintaining plant diversity under changing environmental conditions in seasonally dry and fire‐prone environments? Location: Southwest Western Australia. Methods: Plant species abundance and soil nutrients were determined at 16 forest sites with variable fire histories across an aridity gradient. All plant species were classified based on their functional traits as (1) perennial or annual, (2) ectomycorrhizal, arbuscular mycorrhizal, ericoid mycorrhizal, orchid mycorrhizal, proteoid or other non‐mycorrhizal, (3) resprouters or seeder, and (4) nitrogen fixer or non‐fixer. We used a multivariate (fourth‐corner) technique to simultaneously test the significance and direction of the relationship between each of these traits and fire frequency, fire interval length, aridity, and soil N, P and C fractions. Results: The functional response of the vegetation to fire regime was minor and restricted to annual species, which comprised only ～4% of taxa. Proteoid and ectomycorrhizal species dominated over species with arbuscular and orchid mycorrhizal roots, N‐fixers dominated over non‐fixers, and seeders dominated over resprouters when N fertility was low but organic labile P was high. Further, proteoid and ectomycorrhizal species richness increased with aridity, while arbuscular mycorrhizal species richness decreased. Conclusions: While the functional composition of southwest Australian vegetation is largely insensitive to changes in fire regime, nutrient acquisition and, to a lesser extent, regeneration traits provide mechanisms for the vegetation community to adjust to changes in resource availability. Thus, diversity responses to environmental change in seasonally dry and fire‐prone ecosystems are likely to be primarily mediated by the composition of nutrient acquisition traits in the vegetation community.     

Evolutionary history of fire‐stimulated resprouting,flowering, seed release and germination

Fire has shaped the evolution of many plant traits in fire‐prone environments: fire‐resistant tissues with heat‐insulated meristems, post‐fire resprouting or fire‐killed but regenerating from stored seeds, fire‐stimulated flowering, release of on‐plant‐stored seeds, and germination of soil‐stored seeds. Flowering, seed release and germination fit into three categories of response to intensifying fire: fire not required, weakly fire‐adapted or strongly fire‐adapted. Resprouting also has three categories but survival is always reduced by increasing fire intensity. We collated 286 records for 20 angiosperm and two gymnosperm families and 50 trait assignments to dated phylogenies. We placed these into three fire‐adapted trait types: those associated with the origin of their clade and the onset of fire‐proneness [primary diversification, contributing 20% of speciation events over the last 120 million years (My)], those originating much later coincident with a change in the fire regime (secondary diversification, 30%), and those conserved in the daughter lineage as already adapted to the fire regime (stabilisation, 50%). All four fire‐response types could be traced to >100 My ago (Mya) with pyrogenic flowering slightly younger because of its dependence on resprouting. There was no evidence that resprouting was always an older trait than either seed storage or non‐sprouting throughout this period, with either/both ancestral or derived in different clades and times. Fire‐adapted traits evolved slowly in the Cretaceous, 120–65 Mya, and rapidly but fitfully in the Cenozoic, 65–0 Mya, peaking over the last 20 My. The four trait‐types climaxed at different times, with the peak in resprouter speciation over the last 5 My attributable to fluctuating growing conditions and increasing savanna grasslands unsuitable for non‐sprouters. All experienced a trough in the 40–30‐Mya period following a reduction in world temperatures and oxygen levels and expected reduced fire activity. Thick bark and serotiny arose in the Mid‐Cretaceous among extant Pinaceae. Heat‐stimulated germination of hard seeds is ancestral in the 103‐My‐old Fabales. Smoke‐(karrikin)‐stimulated germination of non‐hard seeds is even older, and includes the 101‐My‐old Restionaceae–Anarthriaceae. A smoke/karrikin response is detectable in some fire‐free lineages that prove to have a fire‐prone ancestry. Among clades that are predominantly fire‐prone, absence of fire‐related traits is the advanced condition, associated either with increased fire frequency (loss of serotiny and soil storage), or migration to fire‐free habitats (loss of thick bark, pyrogenic flowering, serotiny or soil storage). Protea (Africa) and Hakea (Australia) illustrate the importance of stabilisation processes between resprouting/non‐sprouting in accounting for speciation events over the last 20 My and highlight the frequent interchange possible between these two traits. Apart from Pinus, most ancestral trait reconstruction relative to fire has been conducted on predominantly Southern Hemisphere clades and this needs to be redressed. Despite these limitations, it is clear that fire has had a profound effect on fire‐related trait evolution worldwide, and set the platform for subsequent evolution of many non‐fire‐related traits. Genetics of the triggering mechanisms remain poorly understood, except the karrikin system for smoke‐stimulated germination. We exhort biologists to include fire‐proneness and fire‐related traits in their thinking on possible factors controlling the evolution of plants.     

Linking plant genes to insect communities: Identifying the genetic bases of plant traits and community composition

Community genetics aims to understand the effects of intraspecific genetic variation on community composition and diversity, thereby connecting community ecology with evolutionary biology. Thus far, research has shown that plant genetics can underlie variation in the composition of associated communities (e.g., insects, lichen and endophytes), and those communities can therefore be considered as extended phenotypes. This work, however, has been conducted primarily at the plant genotype level and has not identified the key underlying genes. To address this gap, we used genome‐wide association mapping with a population of 445 aspen (Populus tremuloides) genets to identify the genes governing variation in plant traits (defence chemistry, bud phenology, leaf morphology, growth) and insect community composition. We found 49 significant SNP associations in 13 Populus genes that are correlated with chemical defence compounds and insect community traits. Most notably, we identified an early nodulin‐like protein that was associated with insect community diversity and the abundance of interacting foundation species (ants and aphids). These findings support the concept that particular plant traits are the mechanistic link between plant genes and the composition of associated insect communities. In putting the “genes” into “genes to ecosystems ecology”, this work enhances understanding of the molecular genetic mechanisms that underlie plant–insect associations and the consequences thereof for the structure of ecological communities.     

Invasive plants in Minnesota are “joining the locals”: A trait‐based analysis

Questions

Predicting which newly arrived species will establish and become invasive is a problem that has long vexed researchers. In a study of cold temperate oak forest stands, we examined two contrasting hypotheses regarding plant functional traits to explain the success of certain non‐native species. Under the “join the locals” hypothesis, successful invaders are expected to share traits with resident species because they employ successful growth strategies under light‐limited understorey conditions. Instead, under the “try harder” hypothesis, successful invaders are expected to have traits different from native species in order to take advantage of unused niche space.

Location

Minnesota, USA.

Methods

We examined these two theories using 109 native and 11 non‐native plants in 68 oak forest stands. We focused on traits related to plant establishment and growth, including specific leaf area (SLA), leaf carbon‐to‐nitrogen ratio (C:N), wood density, plant maximum height, mycorrhizal type, seed mass and growth form. We compared traits of native and non‐native species using ordinations in multidimensional trait space and compared community‐weighted mean (CWM) trait values across sites.

Results

We found few differences between trait spaces occupied by native and non‐native species. Non‐native species occupied smaller areas of trait space than natives, yet were within that of the native species, indicating similar growth strategies. We observed a higher proportion of non‐native species in sites with higher native woody species CWM SLA and lower CWM C:N. Higher woody CWM SLA was observed in sites with higher soil pH, while lower CWM C:N was found in sites with higher light levels.

Conclusions

Non‐native plants in this system have functional traits similar to natives and are therefore “joining the locals.” However, non‐native plants may possess traits toward the acquisitive end of the native plant trait range, as evidenced by higher non‐native plant abundance in high‐resource environments.

     

Seed and seedling responses to inoculation with mycorrhizal fungi and root nodule bacteria: implications for restoration of degraded Mediterranean‐type Tuart woodlands

Inoculation with beneficial soil microorganisms has the potential to enhance success of restoration, particularly in harsh Mediterranean‐type ecosystems (MTEs). We investigated the effects of microorganisms (mycorrhizal fungi and root nodule bacteria) and planting material (seed and nursery‐raised seedlings) on early establishment and growth of two key postdisturbance colonizing species with different life histories, life forms and functional types (Eucalyptus gomphocephala and Acacia saligna) under field conditions. Establishment and growth were monitored at 13 months, following the first MTE drought period. For E. gomphocephala, establishment was higher for seedlings (81%) than for seeding (7.5%). Inoculation with ectomycorrhizal fungal spores was not beneficial. For A. saligna, establishment was also higher for seedlings (84%) than for seeding (42.5%). Mycorrhizal fungal inoculum had no effect on establishment or growth. This study has shown that in harsh MTE conditions, the use of seedlings is more effective than seeding in degraded woodlands even when attempting to reintroduce key colonizing species. The microorganism treatments tested did not result in significant improvement in establishment or growth.     

Global change and plant–pollinator communities in Mediterranean biomes

Aim

Occurring in five distinct global regions, Mediterranean-type ecosystems (MTEs) include both centres of agricultural production and hotspots of extratropical biodiversity – particularly for plants and bees. Considerable research has addressed the persistence of highly diverse biological communities within MTEs, despite their typically long histories of anthropogenic and natural disturbance. However, important questions remain, especially regarding the limits of ecological resilience in the face of accelerating environmental change. Here, we explore current knowledge regarding the effects of disturbance on MTE plant–pollinator communities.

Location

Mediterranean Basin, California, Cape Province in South Africa, Central Chile and Southern South-Western Australia.

Taxa Studied

Flowering plants and pollinators (insects, birds and mammals).

Methods

We reviewed the available literature about MTE plant–pollinator communities via a systematic search that yielded 234 case studies. We analysed this dataset to quantify research efforts across regions and taxonomic groups, the proportion of surveys addressing ecological interactions (i.e. rather than only taxonomic diversity) and the availability of work addressing community responses to specific stressors (viz. climate change, landscape alteration, fire, farming, grazing, urbanization and species introductions).

Results

Current knowledge on MTE plant–pollinator communities is dominated by work from the northern Mediterranean Basin, while the Southern Hemisphere and California are markedly understudied by comparison. Taxonomic coverage is similarly uneven, with 58% of studies focusing only on a single pollinator group. Furthermore, less than half of the surveys address ecological networks. Finally, despite some pioneering work addressing fire, climate and species introductions, only 13% focus on the impact of stressors on interaction networks.

Outlook

Based on our findings, we identify a need for coordinated international research efforts focusing on (i) community-level studies, observational and experimental, (ii) ecological networks, (iii) functional traits mediating post-disturbance recovery and (iv) impacts of combined/synergistic stressors. Progress in these areas will facilitate predictions about the long-term impacts of global change on MTE plant–pollinator communities.     

Do Mediterranean‐type ecosystems have a common history?—Insights from the Buckthorn family (Rhamnaceae)

Mediterranean‐type ecosystems (MTEs) are remarkable in their species richness and endemism, but the processes that have led to this diversity remain enigmatic. Here, we hypothesize that continent‐dependent speciation and extinction rates have led to disparity in diversity between the five MTEs of the world: the Cape, California, Mediterranean Basin, Chile, and Western Australia. To test this hypothesis, we built a phylogenetic tree for 280 Rhamnaceae species, estimated divergence times using eight fossil calibrations, and used Bayesian methods and simulations to test for differences in diversification rates. Rhamnaceae lineages in MTEs generally show higher diversification rates than elsewhere, but speciation and extinction dynamics show a pattern of continent‐dependence. We detected high speciation and extinction rates in California and significantly lower extinction rates in the Cape and Western Australia. The independent colonization of four of five MTEs may have occurred conterminously in the Oligocene/Early Miocene, but colonization of the Mediterranean Basin happened later, in the Late Miocene. This suggests that the in situ radiations of these clades were initiated before the onset of winter rainfall in these regions. These results indicate independent evolutionary histories of Rhamnaceae in MTEs, possibly related to the intensity of climate oscillations and the geological history of the regions.     

Broad‐scale patterns in smoke‐responsive germination from the south‐eastern Australian flora

Questions

Fire is a crucial component of many ecosystems. Plants whose seeds germinate in response to smoke may benefit from resource availability in the post‐fire environment. Smoke can influence germination timing and success, as well as seedling vigour, resulting in burgeoning research interest in smoke‐responsive germination. Research in this field has largely focused on four key ‘Mediterranean‐type’ fire‐prone ecosystems: the Mediterranean Basin, South African fynbos, Californian chaparral and Western Australia. There are far fewer studies from south‐eastern Australia, a fire‐prone but not “Mediterranean‐type” region. How does smoke‐responsive germination in this region vary according to ecological, phylogenetic, and methodological variables?

Location

South‐eastern Australia.

Methods

We investigated patterns of smoke‐promoted germination in south‐eastern Australian plants across habitat types, growth forms, fire response strategies, phylogeny, taxonomic levels and smoke application methods. We compiled and interrogated data comprising 303 entries on germination responses to smoke in 233 south‐eastern Australian plant species, from 33 different sources.

Results

Smoke‐responsive germination occurs at a lower rate (~41% of tested species) in south‐eastern Australian flora than it does in fynbos and Western Australian floras, and there is clear patterning within these data. Obligate‐seeding species were more likely to respond, Leguminosae and Rubiaceae were less likely to respond (although we question the generality of these results), while Poaceae were more likely to respond to smoke. Finally, studies using aerosol smoke and studies conducted in situ were most likely to find smoke‐promoted germination.

Conclusions

Obligate seeders and Poaceae may be selected for in habitats with higher fire frequencies, consistent with literature suggesting that short inter‐fire intervals favour grasslands over forests. These findings may be particular to south‐eastern Australia, or more widely applicable; more broad‐scale comparative research will reveal the answer. By synthesizing the south‐eastern Australian smoke germination literature we broaden our understanding beyond the better‐studied Mediterranean‐type floras.

     

Origins of female genital diversity: Predation risk and lock‐and‐key explain rapid divergence during an adaptive radiation

The study of male genital diversity has long overshadowed evolutionary inquiry of female genitalia, despite its nontrivial diversity. Here, we identify four nonmutually exclusive mechanisms that could lead to genital divergence in females, and potentially generate patterns of correlated male–female genital evolution: (1) ecological variation alters the context of sexual selection (“ecology hypothesis”), (2) sexually antagonistic selection (“sexual‐conflict hypothesis”), (3) female preferences for male genitalia mediated by female genital traits (“female‐choice hypothesis”), and (4) selection against inter‐population mating (“lock‐and‐key hypothesis”). We performed an empirical investigation of all four hypotheses using the model system of Bahamas mosquitofish inhabiting blue holes that vary in predation risk. We found unequivocal support for the ecology hypothesis, with females exhibiting a smaller genital opening in blue holes containing piscivorous fish. This is consistent with stronger postmating female choice/conflict when predators are present, but greater premating female choice in their absence. Our results additionally supported the lock‐and‐key hypothesis, uncovering a pattern of reproductive character displacement for genital shape. We found no support for the sexual conflict or female choice hypotheses. Our results demonstrate a strong role for ecology in generating female genital diversity, and suggest that lock‐and‐key may provide a viable cause of female genital diversification.     

HOST‐SPECIALIST LINEAGES DOMINATE THE ADAPTIVE RADIATION OF REEF CORAL ENDOSYMBIONTS

Bursts in species diversification are well documented among animals and plants, yet few studies have assessed recent adaptive radiations of eukaryotic microbes. Consequently, we examined the radiation of the most ecologically dominant group of endosymbiotic dinoflagellates found in reef‐building corals, Symbiodinium Clade C, using nuclear ribosomal (ITS2), chloroplast (psbA^ncr), and multilocus microsatellite genotyping. Through a hierarchical analysis of high‐resolution genetic data, we assessed whether ecologically distinct Symbiodinium, differentiated by seemingly equivocal rDNA sequence differences, are independent species lineages. We also considered the role of host specificity in Symbiodinium speciation and the correspondence between endosymbiont diversification and Caribbean paleo‐history. According to phylogenetic, biological, and ecological species concepts, Symbiodinium Clade C comprises many distinct species. Although regional factors contributed to population‐genetic structuring of these lineages, Symbiodinium diversification was mainly driven by host specialization. By combining patterns of the endosymbiont's host specificity, water depth distribution, and phylogeography with paleo‐historical signals of climate change, we inferred that present‐day species diversity on Atlantic coral reefs stemmed mostly from a post‐Miocene adaptive radiation. Host‐generalist progenitors spread, specialized, and diversified during the ensuing epochs of prolonged global cooling and change in reef‐faunal assemblages. Our evolutionary reconstruction thus suggests that Symbiodinium undergoes “boom and bust” phases in diversification and extinction during major climate shifts.     

The influence of range‐wide plant genetic variation on soil invertebrate communities

Plant genetic variation can have far‐reaching effects on associated communities and ecosystems. Heritable variation in ecologically relevant plant traits is often non‐randomly distributed across a species’ range and can exhibit geographic clines. In the event of range expansions and migration, previously unfamiliar genotypes may have large impacts on resident communities and ecosystems due to the introduction of novel and heritable phenotypic variation. Here we test the hypothesis that geographic origin of a focal plant genotype has effects on belowground invertebrate communities using a common garden field experiment. We sampled soil invertebrates from 103 Oenothera biennis genotypes, which were collected from across the species’ range and planted into a common garden field experiment at the northern range limit. We enumerated 24 000 individuals from 190 morphospecies and found that the diversity, abundance, and composition of soil invertebrate communities varied greatly among plant genotypes. Despite strong effects of plant genotype, we found few genetic correlations between plant traits and soil invertebrate community variables. However, herbivore damage was strongly related to variation in the soil invertebrate community. Geographic origin of plant genotypes had at most a weak effect on belowground communities. We speculate that predicting the extended effects of population movement on associated communities will require detailed knowledge of the trait variation occurring within focal species across particular environmental gradients.     

A tale of worldwide success: Behind the scenes of Carex (Cyperaceae) biogeography and diversification

The megadiverse genus Carex (c. 2000 species, Cyperaceae) has a nearly cosmopolitan distribution, displaying an inverted latitudinal richness gradient with higher species diversity in cold‐temperate areas of the Northern Hemisphere. Despite great expansion in our knowledge of the phylogenetic history of the genus and many molecular studies focusing on the biogeography of particular groups during the last few decades, a global analysis of Carex biogeography and diversification is still lacking. For this purpose, we built the hitherto most comprehensive Carex‐dated phylogeny based on three markers (ETS–ITS–matK), using a previous phylogenomic Hyb‐Seq framework, and a sampling of two‐thirds of its species and all recognized sections. Ancestral area reconstruction, biogeographic stochastic mapping, and diversification rate analyses were conducted to elucidate macroevolutionary biogeographic and diversification patterns. Our results reveal that Carex originated in the late Eocene in E Asia, where it probably remained until the synchronous diversification of its main subgeneric lineages during the late Oligocene. E Asia is supported as the cradle of Carex diversification, as well as a “museum” of extant species diversity. Subsequent “out‐of‐Asia” colonization patterns feature multiple asymmetric dispersals clustered toward present times among the Northern Hemisphere regions, with major regions acting both as source and sink (especially Asia and North America), as well as several independent colonization events of the Southern Hemisphere. We detected 13 notable diversification rate shifts during the last 10 My, including remarkable radiations in North America and New Zealand, which occurred concurrently with the late Neogene global cooling, which suggests that diversification involved the colonization of new areas and expansion into novel areas of niche space.     

Environmental filtering predicts plant‐community trait distribution and diversity: Kettle holes as models of meta‐community systems

• Meta‐communities of habitat islands may be essential to maintain biodiversity in anthropogenic landscapes allowing rescue effects in local habitat patches. To understand the species‐assembly mechanisms and dynamics of such ecosystems, it is important to test how local plant‐community diversity and composition is affected by spatial isolation and hence by dispersal limitation and local environmental conditions acting as filters for local species sorting.We used a system of 46 small wetlands (kettle holes)—natural small‐scale freshwater habitats rarely considered in nature conservation policies—embedded in an intensively managed agricultural matrix in northern Germany. We compared two types of kettle holes with distinct topographies (flat‐sloped, ephemeral, frequently plowed kettle holes vs. steep‐sloped, more permanent ones) and determined 254 vascular plant species within these ecosystems, as well as plant functional traits and nearest neighbor distances to other kettle holes.Differences in alpha and beta diversity between steep permanent compared with ephemeral flat kettle holes were mainly explained by species sorting and niche processes and mass effect processes in ephemeral flat kettle holes. The plant‐community composition as well as the community trait distribution in terms of life span, breeding system, dispersal ability, and longevity of seed banks significantly differed between the two habitat types. Flat ephemeral kettle holes held a higher percentage of non‐perennial plants with a more persistent seed bank, less obligate outbreeders and more species with seed dispersal abilities via animal vectors compared with steep‐sloped, more permanent kettle holes that had a higher percentage of wind‐dispersed species. In the flat kettle holes, plant‐species richness was negatively correlated with the degree of isolation, whereas no such pattern was found for the permanent kettle holes.Synthesis: Environment acts as filter shaping plant diversity (alpha and beta) and plant‐community trait distribution between steep permanent compared with ephemeral flat kettle holes supporting species sorting and niche mechanisms as expected, but we identified a mass effect in ephemeral kettle holes only. Flat ephemeral kettle holes can be regarded as meta‐ecosystems that strongly depend on seed dispersal and recruitment from a seed bank, whereas neighboring permanent kettle holes have a more stable local species diversity.

     

Multiple trade‐offs regulate the effects of woody plant removal on biodiversity and ecosystem functions in global rangelands

Woody plant encroachment is a major land management issue. Woody removal often aims to restore the original grassy ecosystem, but few studies have assessed the role of woody removal on ecosystem functions and biodiversity at global scales. We collected data from 140 global studies and evaluated how different woody plant removal methods affected biodiversity (plant and animal diversity) and ecosystem functions (plant production, hydrological function, soil carbon) across global rangelands. Our results indicate that the impact of removal is strongly context dependent, varying with the specific response variable, removal method, and traits of the target species. Over all treatments, woody plant removal increased grass biomass and total groundstorey diversity. Physical and chemical removal methods increased grass biomass and total groundstorey biomass (i.e., non‐woody plants, including grass biomass), but burning reduced animal diversity. The impact of different treatment methods declined with time since removal, particularly for total groundstorey biomass. Removing pyramid‐shaped woody plants increased total groundstorey biomass and hydrological function but reduced total groundstorey diversity. Environmental context (e.g., aridity and soil texture) indirectly controlled the effect of removal on biomass and biodiversity by influencing plant traits such as plant shape, allelopathic, or roots types. Our study demonstrates that a one‐size‐fits‐all approach to woody plant removal is not appropriate, and that consideration of woody plant identity, removal method, and environmental context is critical for optimizing removal outcomes. Applying this knowledge is fundamental for maintaining diverse and functional rangeland ecosystems as we move toward a drier and more variable climate.     

Diversity and salt tolerance of native Acacia rhizobia isolated from saline and non‐saline soils

Re‐establishing native vegetation in stressed soils is of considerable importance in many parts of the world, leading to significant interest in using plant–soil symbiont interactions to increase the cost‐effectiveness of large‐scale restoration. However, effective use of soil microbes in revegetation requires knowledge of how microbe communities vary along environmental stress gradients, as well as how such variation relates to symbiont effectiveness. In Australia, shrubby legumes dominate many ecosystems where dryland salinity is a major issue, and improving plant establishment in saline soils is a priority of regional management agencies. In this study, strains of rhizobial bacteria were isolated from a range of Acacia spp. growing in saline and non‐saline soils. Replicates of each strain were grown under several salinity levels in liquid culture and characterized for growth and salt tolerance. Genetic characterization of rhizobia showed considerable variation among strains, with salt tolerance and growth generally higher in rhizobial populations derived from more saline soils. These strains showed markedly different genetic profiles and generic affiliations to those from more temperate soils, suggesting community differentiation in relation to salt stress. The identification of novel genomic species from saline soils suggests that the diversity of rhizobia associated with Australian Acacia spp. is significantly greater than previously described. Overall, the ability of some symbiotically effective strains to tolerate high salinity is promising with regard to improving host plant re‐establishment in these soils.