A novel type of nutritional ant-plant interaction: ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna.

Many plants combat herbivore and pathogen attack indirectly by attracting predators of their herbivores. Here we describe a novel type of insect-plant interaction where a carnivorous plant uses such an indirect defence to prevent nutrient loss to kleptoparasites. The ant Camponotus schmitzi is an obligate inhabitant of the carnivorous pitcher plant Nepenthes bicalcarata in Borneo. It has recently been suggested that this ant-plant interaction is a nutritional mutualism, but the detailed mechanisms and the origin of the ant-derived nutrient supply have remained unexplained. We confirm that N. bicalcarata host plant leaves naturally have an elevated (15)N/(14)N stable isotope abundance ratio (δ(15)N) when colonised by C. schmitzi. This indicates that a higher proportion of the plants' nitrogen is insect-derived when C. schmitzi ants are present (ca. 100%, vs. 77% in uncolonised plants) and that more nitrogen is available to them. We demonstrated direct flux of nutrients from the ants to the host plant in a (15)N pulse-chase experiment. As C. schmitzi ants only feed on nectar and pitcher contents of their host, the elevated foliar δ(15)N cannot be explained by classic ant-feeding (myrmecotrophy) but must originate from a higher efficiency of the pitcher traps. We discovered that C. schmitzi ants not only increase the pitchers' capture efficiency by keeping the pitchers' trapping surfaces clean, but they also reduce nutrient loss from the pitchers by predating dipteran pitcher inhabitants (infauna). Consequently, nutrients the pitchers would have otherwise lost via emerging flies become available as ant colony waste. The plants' prey is therefore conserved by the ants. The interaction between C. schmitzi, N. bicalcarata and dipteran pitcher infauna represents a new type of mutualism where animals mitigate the damage by nutrient thieves to a plant

Evolutionary footprints of a cold relic in a rapidly warming world

With accelerating global warming, understanding the evolutionary dynamics of plant adaptation to environmental change is increasingly urgent. Here we reveal the enigmatic history of the genus Cochlearia (Brassicaceae), a Pleistocene relic that originated from a drought-adapted Mediterranean sister genus during the Miocene. Cochlearia rapidly diversified and adapted to circum-Arctic regions and other cold-characterized habitat types during the Pleistocene. This sudden change in ecological preferences was accompanied by a highly complex, reticulate polyploid evolution, which was apparently triggered by the impact of repeated Pleistocene glaciation cycles. Our results illustrate that two early diversified arctic-alpine diploid gene pools contributed differently to the evolution of this young polyploid genus now captured in a cold-adapted niche. Metabolomics revealed central carbon metabolism responses to cold in diverse species and ecotypes, likely due to continuous connections to cold habitats that may have facilitated widespread adaptation to alpine and subalpine habitats, and which we speculate were coopted from existing drought adaptations. Given the growing scientific interest in adaptive evolution of temperature-related traits, our results provide much-needed taxonomic and phylogenomic resolution of a model system as well as first insights into the origins of its adaptation to cold

Introgression is widespread in the radiation of carnivorous Nepenthes pitcher plants

ISSN:1055-7903ISSN:1095-951

Sex is determined by XY chromosomes across the radiation of dioecious Nepenthes pitcher plants

Species with separate sexes (dioecy) are a minority among flowering plants, but dioecy has evolved multiple times independently in their history. The sex‐determination system and sex‐linked genomic regions are currently identified in a limited number of dioecious plants only. Here, we study the sex‐determination system in a genus of dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD‐seq and sequenced a male inflorescence transcriptome. We developed a statistical tool (privacy rarefaction) to distinguish true sex specificity from stochastic noise in read coverage of sequencing data from wild populations and identified male‐specific loci and XY‐patterned single nucleotide polymorphsims (SNPs) in all three Nepenthes taxa, suggesting the presence of homomorphic XY sex chromosomes. The male‐specific region of the Y chromosome showed little conservation among the three taxa, except for the essential pollen development gene DYT1 that was confirmed as male specific by PCR in additional Nepenthes taxa. Hence, dioecy and part of the male‐specific region of the Nepenthes Y‐chromosomes likely have a single evolutionary origin

Population Genomics of the “Arcanum” Species Group in Wild Tomatoes: Evidence for Separate Origins of Two Self-Compatible Lineages

Given their diverse mating systems and recent divergence, wild tomatoes (Solanum section Lycopersicon) have become an attractive model system to study ecological divergence, the build-up of reproductive barriers, and the causes and consequences of the breakdown of self-incompatibility. Here we report on a lesser-studied group of species known as the “Arcanum” group, comprising the nominal species Solanum arcanum, Solanum chmielewskii, and Solanum neorickii. The latter two taxa are self-compatible but are thought to self-fertilize at different rates, given their distinct manifestations of the morphological “selfing syndrome.” Based on experimental crossings and transcriptome sequencing of a total of 39 different genotypes from as many accessions representing each species’ geographic range, we provide compelling evidence for deep genealogical divisions within S. arcanum; only the self-incompatible lineage known as “var. marañón” has close genealogical ties to the two self-compatible species. Moreover, there is evidence under multiple inference schemes for different geographic subsets of S. arcanum var. marañón being closest to S. chmielewskii and S. neorickii, respectively. To broadly characterize the population-genomic consequences of these recent mating-system transitions and their associated speciation events, we fit demographic models indicating strong reductions in effective population size, congruent with reduced nucleotide and S-locus diversity in the two independently derived self-compatible species.ISSN:1664-462

Samples taken for the analysis of the natural abundance of ¹⁵N in <i>N. bicalcarata</i> phytotelm food webs.

<p>Each of the ten pitchers grew on a different plant, and food web components were sampled and analysed from each pitcher separately. “Other larvae” refers to Brachycera and putative non-predatory Nematocera.</p

Adult infauna emerged from <i>N. bicalcarata</i> pitchers. Unless otherwise stated, values are total numbers of individuals.

<p>Adult infauna emerged from <i>N. bicalcarata</i> pitchers. Unless otherwise stated, values are total numbers of individuals.</p

Flux of nitrogen from ant colony to pitcher plant.

<p>Bars indicate the change in ¹⁵N abundance in the leaves of a <i>N. bicalcarata</i> plant two weeks after feeding a ¹⁵N pulse to the symbiotic <i>C. schmitzi</i> colony. Leaf node 1 bears the youngest leaf. The pictogrammes under the graph explain the structure of the host plant, its ant colony and mark where tracer was fed.</p

Schematic of “emergence trap” for pitcher plant infauna.

<p>The lower bottle containing the pitcher is completely darkened, causing emerging dipterans to move upwards towards the light shining through the neck. Tanglefoot® prevents crawling insects from entering the collection bottle. The fish trap-like design prevents escape from the collection bottle. Emerging insects reaching the collection bottle were killed when falling into a 1.5% CuSO₄ solution. Traps were stabilised with a pole. Whole, living pitchers could be used without significant interference. Although <i>C. schmitzi</i> could freely pass through a small gap in the bottle along the pitcher tendril, the trap was mosquito-tight (without ants, all the 20 inserted individuals were always recovered; n = 10 traps).</p