Reproductive phenology of Melastomataceae species with contrasting reproductive systems: contemporary and historical drivers

• Flowering and fruiting are key events in the life history of plants, and both are critical to their reproductive success. Besides the role of evolutionary history, plant reproductive phenology is regulated by abiotic factors and shaped by biotic interactions with pollinators and seed dispersers. In Melastomataceae, a dominant Neotropical family, the reproductive systems vary from allogamous with biotic pollination to apomictic, and seed dispersal varies from dry (self‐dispersed) to fleshy (animal‐dispersed) fruits. Such variety in reproductive strategies is likely to affect flowering and fruiting phenologies.
• In this study, we described the reproductive phenology of 81 Melastomataceae species occurring in two biodiversity hotspots: the Atlantic rain forest and the campo rupestre. We aim to disentangle the role of abiotic and biotic factors defining flowering and fruiting times of Melastomataceae species, considering the contrasting breeding and seed dispersal systems, and their evolutionary history.
• In both vegetation types, pollinator‐dependent species had higher flowering seasonality than pollinator‐independent ones. Flowering patterns presented phylogenetic signal regardless of vegetation type. Fruiting of fleshy‐fruited species was seasonal in campo rupestre but not in Atlantic rain forest; the fruiting of dry‐fruited species was also not seasonal in both vegetation types. Fruiting showed a low phylogenetic signal, probably because the influence of environment and dispersal agents on fruiting time is stronger than the phylogenetic affinity.
• Considering these ecophylogenetic patterns, our results indicate that flowering may be shaped by the different reproductive strategies of Melastomataceae lineages, while fruiting patterns may be governed mainly by the seed dispersal strategy and flowering time, with less phylogenetic influence.

     

Forest phenology and a warmer climate – growing season extension in relation to climatic provenance

Predicting forest responses to warming climates relies on assumptions about niche and temperature sensitivity that remain largely untested. Observational studies have related current and historical temperatures to phenological shifts, but experimental evidence is sparse, particularly for autumn responses. A 4 year field experiment exposed four deciduous forest species from contrasting climates (Liquidambar styraciflua, Quercus rubra, Populus grandidentata, and Betula alleghaniensis) to air temperatures 2 and 4 °C above ambient controls, using temperature‐controlled open top chambers. Impacts of year‐round warming on bud burst (BB), senescence, and abscission were evaluated in relation to thermal provenance. Leaves emerged earlier in all species by an average of 4–9 days at +2 °C and 6–14 days at +4 °C. Magnitude of advance varied with species and year, but was larger for the first 2 °C increment than for the second. Effect of warming increased with early BB, favoring Liquidambar, but even BB of northern species advanced, despite temperatures exceeding those of the realized niche. Treatment differences in BB were inadequately explained by temperature sums alone. In autumn, chlorophyll was retained an average of 4 and 7 days longer in +2 and +4 °C treatments, respectively, and abscission delayed by 8 and 13 days. Growing seasons in the warmer atmospheres averaged 5–18 days (E2) and 6–28 days (E4) longer, according to species, with the least impact in Quercus. Results are compared with a 16 years record of canopy onset and offset in a nearby upland deciduous forest, where BB showed similar responsiveness to spring temperatures (2–4 days °C^?1). Offset dates in the stand tracked August–September temperatures, except when late summer drought caused premature senescence. The common garden‐like experiment provides evidence that warming alone extends the growing season, at both ends, even if stand‐level impacts may be complicated by variation in other environmental factors.     

Contributions of climate,plant phenology and natural enemies to the seasonal variation of aphids on cabbage

Brevicoryne brassicae (L), Lipaphis erysimi (Kalt) and Myzus persicae (Sultzer) (Homoptera: Aphididae) form the aphid complex that causes great losses in Brassicaceae in tropical and subtropical regions. Knowledge of their population dynamics is important for the development of integrated pest management programmes. This study aimed to investigate the effects of cabbage phenology, climatic factors and natural enemies populations on the dynamics of these organisms, and the factors regulating their predators’ occurrence. The densities of aphids and their natural enemies and the climate were monitored for two years in 16 cabbage crops. The highest densities of the aphids occurred during periods of relative humidity (RH) drop, a condition that affects them positively. Regarding the predators, the factors affecting their abundance varied but RH was positively related to most of them. This study provides relevant insights into the factors that regulate the aphids in cabbage and for the decision‐making process of control of these severe pests.     

Evolution,plasticity and evolving plasticity of phenology in the tree species Alnus glutinosa

Both traits and the plasticity of these traits are subject to evolutionary change and therefore affect the long‐term persistence of populations and their role in local communities. We subjected clones from 12 different populations of Alnus glutinosa, located along a latitudinal gradient, to two different temperature treatments, to disentangle the distribution of genetic variation in timing of bud burst and bud burst plasticity within and among genotypes, populations, and regions. We calculated heritability and evolvability estimates for bud burst and bud burst plasticity and assessed the influence of divergent selection relative to neutral drift. We observed higher levels of heritability and evolvability for bud burst than for its plasticity, whereas the total phenological heritability and evolvability (i.e. combining timing of bud burst and bud burst plasticity) suggest substantial evolutionary potential with respect to phenology. Earlier bud burst was observed for the low‐latitudinal populations than for the populations from higher latitudes, whereas the high‐latitudinal populations did not show the expected delayed bud burst. This countergradient variation can be due to evolution towards increased phenological plasticity at higher latitudes. However, because we found little evidence for adaptive differences in phenological plasticity across the latitudinal gradient, we suggest differential frost tolerance as the most likely explanation for the observed phenological patterns in A. glutinosa.     

Cascading effects of climate extremes on vertebrate fauna through changes to low‐latitude tree flowering and fruiting phenology

Forest vertebrate fauna provide critical services, such as pollination and seed dispersal, which underpin functional and resilient ecosystems. In turn, many of these fauna are dependent on the flowering phenology of the plant species of such ecosystems. The impact of changes in climate, including climate extremes, on the interaction between these fauna and flora has not been identified or elucidated, yet influences on flowering phenology are already evident. These changes are well documented in the mid to high latitudes. However, there is emerging evidence that the flowering phenology, nectar/pollen production, and fruit production of long‐lived trees in tropical and subtropical forests are also being impacted by changes in the frequency and severity of climate extremes. Here, we examine the implications of these changes for vertebrate fauna dependent on these resources. We review the literature to establish evidence for links between climate extremes and flowering phenology, elucidating the nature of relationships between different vertebrate taxa and flowering regimes. We combine this information with climate change projections to postulate about the likely impacts on nectar, pollen and fruit resource availability and the consequences for dependent vertebrate fauna. The most recent climate projections show that the frequency and intensity of climate extremes will increase during the 21st century. These changes are likely to significantly alter mass flowering and fruiting events in the tropics and subtropics, which are frequently cued by climate extremes, such as intensive rainfall events or rapid temperature shifts. We find that in these systems the abundance and duration of resource availability for vertebrate fauna is likely to fluctuate, and the time intervals between episodes of high resource availability to increase. The combined impact of these changes has the potential to result in cascading effects on ecosystems through changes in pollinator and seed dispersal ecology, and demands a focused research effort.     

Risk of genetic maladaptation due to climate change in three major European tree species

Tree populations usually show adaptations to their local environments as a result of natural selection. As climates change, populations can become locally maladapted and decline in fitness. Evaluating the expected degree of genetic maladaptation due to climate change will allow forest managers to assess forest vulnerability, and develop strategies to preserve forest health and productivity. We studied potential genetic maladaptation to future climates in three major European tree species, Norway spruce (Picea abies), silver fir (Abies alba), and European beech (Fagus sylvatica). A common garden experiment was conducted to evaluate the quantitative genetic variation in growth and phenology of seedlings from 77 to 92 native populations of each species from across Switzerland. We used multivariate genecological models to associate population variation with past seed source climates, and to estimate relative risk of maladaptation to current and future climates based on key phenotypic traits and three regional climate projections within the A1B scenario. Current risks from climate change were similar to average risks from current seed transfer practices. For all three climate models, future risks increased in spruce and beech until the end of the century, but remained low in fir. Largest average risks associated with climate projections for the period 2061–2090 were found for spruce seedling height (0.64), and for beech bud break and leaf senescence (0.52 and 0.46). Future risks for spruce were high across Switzerland. However, areas of high risk were also found in drought‐prone regions for beech and in the southern Alps for fir. Genetic maladaptation to future climates is likely to become a problem for spruce and beech by the end of this century, but probably not for fir. Consequently, forest management strategies should be adjusted in the study area for spruce and beech to maintain productive and healthy forests in the future.     

Using species distribution models to select species resistant to climate change for ecological restoration of bowé in West Africa

Bowalization is a particular form of land degradation and leads to lateral expansion of ferricrete horizons. The process occurs only in tropical regions. In this study, the most adapted and resistant species towards climate change were identified on bowé. The 15 most common bowé species of the subhumid and semi‐arid climate zones of Benin were submitted together with significant environmental variables (elevation, current bioclimatic variables, soil types) to three ecological niche modelling programmes (Maxent, Domain and GARP). For future prediction (2050), IPCC4/CIAT and IPCC5/CMIP5 climate data were applied. Asparagus africanus, Andropogon pseudapricus and Combretum nigricans were identified as the most resistant species for ecological restoration of bowé in the semi‐arid climate zone and Asparagus africanus, Detarium microcarpum and Lannea microcarpa in the subhumid climate zone. The ‘Pull’ strategies were identified as appropriate for ecological restoration of bowé in Benin.     

Response of two parasitoid species (Hymenoptera: Braconidae,Figitidae) to tephritid host and host food substrate cues

The Neotropical‐native figitid Aganaspis pelleranoi (Brèthes) and the Asian braconid Diachasmimorpha longicaudata (Ashmead) are two parasitoids of Tephritidae fruit flies with long and recent, respectively, evolutionary histories in the Neotropics. Both species experienced a recent range of overlap. In Argentina, A. pelleranoi is a potential species in biological control programs against the pestiferous tephritid species, Anastrepha fraterculus (Wiedemann) and Ceratitis capitata (Wiedemann), whereas D. longicaudata is already used in open‐field releases against Medfly in central‐western Argentina. To characterize the host‐foraging strategies of A. pelleranoi and D. longicaudata, olfactometer experiments were conducted comparing responses to C. capitata and A. fraterculus larvae, in two kinds of food substrate: fruit and artificial larval medium. To control the possible influence of host larvae used for parasitoid rearing on olfactory response, two strains of both parasitoid species, reared on both tephrtid species, were studied. Volatiles directly emanating either from A. fraterculus or C. capitata larvae may be detected by both A. pelleranoi and D. longicaudata, although chemical stimuli originating from the combination of host larvae and the habitat of the host were preferred. However, olfactory cues associated with host larvae probably play a relevant role in host searching behaviour of A. pelleranoi, whereas for D. longicaudata, the host‐habitat olfactory stimuli would be highly essential in short‐range host location. The strain of the parasitoids did not affect host search ability on the two tephritid species evaluated. These evidences are relevant for mass production of both parasitoids and their impact following open‐field augmentative releases.     

Adaptive and plastic responses of Quercus petraea populations to climate across Europe

How temperate forests will respond to climate change is uncertain; projections range from severe decline to increased growth. We conducted field tests of sessile oak (Quercus petraea), a widespread keystone European forest tree species, including more than 150 000 trees sourced from 116 geographically diverse populations. The tests were planted on 23 field sites in six European countries, in order to expose them to a wide range of climates, including sites reflecting future warmer and drier climates. By assessing tree height and survival, our objectives were twofold: (i) to identify the source of differential population responses to climate (genetic differentiation due to past divergent climatic selection vs. plastic responses to ongoing climate change) and (ii) to explore which climatic variables (temperature or precipitation) trigger the population responses. Tree growth and survival were modeled for contemporary climate and then projected using data from four regional climate models for years 2071–2100, using two greenhouse gas concentration trajectory scenarios each. Overall, results indicated a moderate response of tree height and survival to climate variation, with changes in dryness (either annual or during the growing season) explaining the major part of the response. While, on average, populations exhibited local adaptation, there was significant clinal population differentiation for height growth with winter temperature at the site of origin. The most moderate climate model (HIRHAM5‐EC; rcp4.5) predicted minor decreases in height and survival, while the most extreme model (CCLM4‐GEM2‐ES; rcp8.5) predicted large decreases in survival and growth for southern and southeastern edge populations (Hungary and Turkey). Other nonmarginal populations with continental climates were predicted to be severely and negatively affected (Bercé, France), while populations at the contemporary northern limit (colder and humid maritime regions; Denmark and Norway) will probably not show large changes in growth and survival in response to climate change.     

Architecture of Iberian canopy tree species in relation to wood density,shade tolerance and climate

Tree architecture has important consequences for tree performance as it determines resource capture, mechanical stability and dominance over competitors. We analyzed architectural relationships between stem and crown dimensions for 13 dominant Iberian canopy tree species belonging to the Pinaceae (six Pinus species) and Fagaceae (six Quercus species and Fagus sylvatica) and related these architectural traits to wood density, shade tolerance and climatic factors. Fagaceae had, compared with Pinaceae, denser wood, saplings with wider crowns and adults with larger maximal crown size but smaller maximal height. In combination, these traits enhance light acquisition and persistence in shaded environments; thus, contributing to their shade tolerance. Pinaceae species, in contrast, had low-density wood, allocate more resources to the formation of the central trunk rather than to branches and attained taller maximal heights, allowing them to grow rapidly in height and compete for light following disturbances; thus, contributing to their high light requirements. Wood density had a strong relationship with tree architecture, with dense-wooded species having smaller maximum height and wider crowns, probably because of cheaper expansion costs for producing biomechanically stable branches. Species from arid environments had shorter stems and shallower crowns for a given stem diameter, probably to reduce hydraulic path length and assure water transport. Wood density is an important correlate of variation in tree architecture between species and the two dominant families, with potentially large implications for their resource foraging strategies and successional dynamics.     

Effective population size as a driver for divergence of an antimicrobial peptide (Hymenoptaecin) in two common European bumblebee species

Social insects are the target of numerous pathogens. This is because the high density of closely‐related individuals frequently interacting with each other enhances the transmission and establishment of pathogens. This high selective pressure results in the rapid evolution of immune genes, which might be counteracted by a reduced effective population size (N_e) lowering the effectiveness of selection. We tested the effect of N_e on the evolutionary rate of an important immune gene for the antimicrobial peptide Hymenoptaecin in two common central European bumblebee species: Bombus terrestris and Bombus lapidarius. Both species are similar in their biology and are expected to be under similar selective pressures because pathogen prevalence does not differ between species. However, previous studies indicated a higher N_e in B. terrestris compared to B. lapidarius. We found high intraspecific variability in the coding sequence but low variability for silent polymorphisms in B. lapidarius. Estimates of long‐ and short‐term N_e were three‐ to four‐fold higher N_e in B. terrestris, although the species did not differ in census population sizes. The difference in N_e might result in less efficient selection and suboptimal adaptation of immune genes (e.g. hymenoptaecin) in B. lapidarius, and thus this species might become less resistant and more tolerant, turning into a superspreader of diseases.     

Big eucalypts grow more slowly in a warm climate: evidence of an interaction between tree size and temperature

Large trees are critical components of forest ecosystems, but are declining in many forests worldwide. We predicted that growth of large trees is more vulnerable than that of small trees to high temperatures, because respiration and tissue maintenance costs increase with temperature more rapidly than does photosynthesis and these costs may be disproportionately greater in large trees. Using 5 00 000 measurements of eucalypt growth across temperate Australia, we found that high temperatures do appear to impose a larger growth penalty on large trees than on small ones. Average stem diameter growth rates at 21 °C compared with 11 °C mean annual temperature were 57% lower for large trees (58 cm stem diameter), but only 29% lower for small trees (18 cm diameter). While our results are consistent with an impaired carbon budget for large trees at warmer sites, we cannot discount causes such as hydraulic stress. We conclude that slower growth rates will impede recovery from extreme events, exacerbating the effects of higher temperatures, increased drought stress and more frequent fire on the tall eucalypt forests of southern Australia.     

Differences in seasonal survival suggest species‐specific reactions to climate change in two sympatric bat species

Long‐lived animals with a low annual reproductive output need a long time to recover from population crashes and are, thus, likely to face high extinction risk, if the current global environmental change will increase mortality rates. To aid conservation of those species, knowledge on the variability of mortality rates is essential. Unfortunately, however, individual‐based multiyear data sets that are required for that have only rarely been collected for free‐ranging long‐lived mammals. Here, we used a five‐year data set comprising activity data of 1,445 RFID‐tagged individuals of two long‐lived temperate zone bat species, Natterer's bats (Myotis nattereri) and Daubenton's bats (Myotis daubentonii), at their joint hibernaculum. Both species are listed as being of high conservation interest by the European Habitats Directive. Applying mixed‐effects logistic regression, we explored seasonal survival differences in these two species which differ in foraging strategy and phenology. In both species, survival over the first winter of an individual's life was much lower than survival over subsequent winters. Focussing on adults only, seasonal survival patterns were largely consistent with higher winter and lower summer survival but varied in its level across years in both species. Our analyses, furthermore, highlight the importance of species‐specific time periods for survival. Daubenton's bats showed a much stronger difference in survival between the two seasons than Natterer's bats. In one exceptional winter, the population of Natterer's bats crashed, while the survival of Daubenton's bats declined only moderately. While our results confirm the general seasonal survival pattern typical for hibernating mammals with higher winter than summer survival, they also show that this pattern can be reversed under particular conditions. Overall, our study points toward a high importance of specific time periods for population dynamics and suggests species‐, population‐, and age class‐specific responses to global climate change.     

Haploid,diploid, and pooled exome capture recapitulate features of biology and paralogy in two non-model tree species

Despite their suitability for studying evolution, many conifer species have large and repetitive giga-genomes (16–31 Gbp) that create hurdles to producing high coverage SNP data sets that capture diversity from across the entirety of the genome. Due in part to multiple ancient whole genome duplication events, gene family expansion and subsequent evolution within Pinaceae, false diversity from the misalignment of paralog copies creates further challenges in accurately and reproducibly inferring evolutionary history from sequence data. Here, we leverage the cost-saving benefits of pool-seq and exome-capture to discover SNPs in two conifer species, Douglas-fir (Pseudotsuga menziesii var. menziesii (Mirb.) Franco, Pinaceae) and jack pine (Pinus banksiana Lamb., Pinaceae). We show, using minimal baseline filtering, that allele frequencies estimated from pooled individuals show a strong, positive correlation with those estimated by sequencing the same population as individuals (r > .948), on par with such comparisons made in model organisms. Further, we highlight the utility of haploid megagametophyte tissue for identifying sites that are probably due to misaligned paralogs. Together with additional minor filtering, we show that it is possible to remove many of the loci with large frequency estimate discrepancies between individual and pooled sequencing approaches, improving the correlation further (r > .973). Our work addresses bioinformatic challenges in non-model organisms with large and complex genomes, highlights the use of megagametophyte tissue for the identification of paralogous artefacts, and suggests the combination of pool-seq and exome capture to be robust for further evolutionary hypothesis testing in these systems.     

Contrasting responses to climate change at Himalayan treelines revealed by population demographics of two dominant species

1. Alpine treelines are expected to shift upward due to recent climate change. However, interpretation of changes in montane systems has been problematic because effects of climate change are frequently confounded with those of land use changes. The eastern Himalaya, particularly Langtang National Park, Central Nepal, has been relatively undisturbed for centuries and thus presents an opportunity for studying climate change impacts on alpine treeline uncontaminated by potential confounding factors.
2. We studied two dominant species, Abies spectabilis (AS) and Rhododendron campanulatum (RC), above and below the treeline on two mountains. We constructed 13 transects, each spanning up to 400 m in elevation, in which we recorded height and state (dead or alive) of all trees, as well as slope, aspect, canopy density, and measures of anthropogenic and animal disturbance.
3. All size classes of RC plants had lower mortality above treeline than below it, and young RC plants (<2 m tall) were at higher density above treeline than below. AS shows little evidence of a position change from the historic treeline, with a sudden extreme drop in density above treeline compared to below. Recruitment, as measured by size–class distribution, was greater above treeline than below for both species but AS is confined to ~25 m above treeline whereas RC is luxuriantly growing up to 200 m above treeline.
4. Synthesis. Evidence suggests that the elevational limits of RC have shifted upward both because (a) young plants above treeline benefited from facilitation of recruitment by surrounding vegetation, allowing upward expansion of recruitment, and (b) temperature amelioration to mature plants increased adult survival. We predict that the current pure stand of RC growing above treeline will be colonized by AS that will, in turn, outshade and eventually relegate RC to be a minor component of the community, as is the current situation below the treeline.

     

The success of assisted colonization and assisted gene flow depends on phenology

Global warming will jeopardize the persistence and genetic diversity of many species. Assisted colonization, or the movement of species beyond their current range boundary, is a conservation strategy proposed for species with limited dispersal abilities or adaptive potential. However, species that rely on photoperiodic and thermal cues for development may experience conflicting signals if transported across latitudes. Relocating multiple, distinct populations may remedy this quandary by expanding genetic variation and promoting evolutionary responses in the receiving habitat – a strategy known as assisted gene flow. To better inform these policies, we planted seeds from latitudinally distinct populations of the annual legume, Chamaecrista fasciculata, in a potential future colonization site north of its current range boundary. Plants were exposed to ambient or elevated temperatures via infrared heating. We monitored several life history traits and estimated patterns of natural selection to determine the adaptive value of plastic responses. To assess the feasibility of assisted gene flow between phenologically distinct populations, we counted flowers each day and estimated the degree of temporal isolation between populations. Increased temperatures advanced each successive phenological trait more than the last, resulting in a compressed life cycle for all but the southern‐most population. Warming altered patterns of selection on flowering onset and vegetative biomass. Population performance was dependent on latitude of origin, with the northern‐most population performing best under ambient conditions and the southern‐most performing most poorly, even under elevated temperatures. Among‐population differences in flowering phenology limited the potential for genetic exchange among the northern‐ and southern‐most populations. All plastic responses to warming were neutral or adaptive; however, photoperiodic constraints will likely necessitate evolutionary responses for long‐term persistence, especially when involving populations from disparate latitudes. With strategic planning, our results suggest that assisted colonization and assisted gene flow may be feasible options for preservation.