Jiaxing Huang

Unveiling cryptic species of the bumblebee subgenus Bombus s. str. worldwide with COI barcodes (Hymenoptera: Apidae)

Bumblebees of the subgenus Bombus s. str. dominate (or used to dominate) many north temperate pollinator assemblages and include most of the commercial bumblebee pollinator species. Several species are now in serious decline, so conservationists need to know precisely which ones are involved. The problem is that many Bombus s. str. species are cryptic, so that species identification from morphology may be impossible for some individuals and is frequently misleading according to recent molecular studies. This is the first review of the entire subgenus to: (1) avoid fixed a priori assumptions concerning the limits of the problematic species; and (2) sample multiple sites from across the entire geographic ranges of all of the principal named taxa worldwide; and (3) fit an explicit model for how characters change within an evolutionary framework; and (4) apply explicit and consistent criteria within this evolutionary framework for recognising species. We analyse easily-obtained DNA (COI-barcode) data for 559 sequences from 279 localities in 33 countries using general mixed Yule-coalescent (GMYC) models, assuming only the morphologically distinctive species B. affinis Cresson, B. franklini (Frison), B. ignitus Smith and B. tunicatus Smith, and then recognise other comparable COI-barcode groups as putative species. These species correspond to modified concepts of the taxa B. cryptarum (Fabricius), B. hypocrita Pérez, B. jacobsoni Skorikov, B. lantschouensis Vogt n. stat., B. longipennis Friese, B. lucorum (Linnaeus), B. magnus Vogt, B. minshanensis Bischoff n. stat., B. occidentalis Greene, B. patagiatus Nylander, B. sporadicus Nylander, B. terrestris (Linnaeus) and B. terricola Kirby (a total of 17 species). Seven lectotypes are designated. Our results allow us for the first time to diagnose all of the putative species throughout their global ranges and to map the extent of these geographic ranges.

Cryptic bumblebee species: consequences for conservation and the trade in greenhouse pollinators.

Commercial greenhouse growers in both Japan and China are increasingly using reared orange-tailed bumblebees known previously as Bombus hypocrita Pérez as pollinators. Phylogenetic analysis of the DNA (COI) barcodes with Bayesian methods shows that this “species” is a long-standing confusion of two cryptic species. We find that the orange-tailed bumblebees in North China are actually part of the widespread Russian (otherwise white-tailed) B. patagiatus Nylander (as B. patagiatus ganjsuensis Skorikov, n. comb.), whereas the orange-tailed bees in Japan are true B. hypocrita. This situation has been further complicated because two other cryptic species from North China that were previously confused with the Russian B. patagiatus are now recognised as separate: B. lantschouensis Vogt n. stat. and B. minshanensis Bischoff n. stat.. As demand for pollination services by greenhouse growers inevitably increases, these bees are more likely to be transported between countries. In order to conserve genetic resources of pollinator species for their option value for future food security, we advocate preventing trade and movement of B. patagiatus from China into Japan and of B. hypocrita from Japan into China.

Managed Bumblebees Outperform Honeybees in Increasing Peach Fruit Set in China: Different Limiting Processes with Different Pollinators

Peach Prunus persica (L.) Batsch is self-compatible and largely self-fertile, but under greenhouse conditions pollinators must be introduced to achieve good fruit set and quality. Because little work has been done to assess the effectiveness of different pollinators on peach trees under greenhouse conditions, we studied ‘Okubo’ peach in greenhouse tunnels near Beijing between 2012 and 2014. We measured pollen deposition, pollen-tube growth rates, ovary development, and initial fruit set after the flowers were visited by either of two managed pollinators: bumblebees, Bombus patagiatus Nylander, and honeybees, Apis mellifera L. The results show that B. patagiatus is more effective than A. mellifera as a pollinator of peach in greenhouses because of differences in two processes. First, B. patagiatus deposits more pollen grains on peach stigmas than A. mellifera, both during a single visit and during a whole day of open pollination. Second, there are differences in the fertilization performance of the pollen deposited. Half of the flowers visited by B. patagiatus are fertilized 9–11 days after bee visits, while for flowers visited by A. mellifera, half are fertilized 13–15 days after bee visits. Consequently, fruit development is also accelerated by bumblebees, showing that the different pollinators have not only different pollination efficiency, but also influence the subsequent time course of fertilization and fruit set. Flowers visited by B. patagiatus show faster ovary growth and ultimately these flowers produce more fruit. Our work shows that pollinators may influence fruit production beyond the amount of pollen delivered. We show that managed indigenous bumblebees significantly outperform introduced honeybees in increasing peach initial fruit set under greenhouse conditions.

Genes Suggest Ancestral Colour Polymorphisms Are Shared across Morphologically Cryptic Species in Arctic Bumblebees.

Our grasp of biodiversity is fine-tuned through the process of revisionary taxonomy. If species do exist in nature and can be discovered with available techniques, then we expect these revisions to converge on broadly shared interpretations of species. But for the primarily arctic bumblebees of the subgenus Alpinobombus of the genus Bombus, revisions by some of the most experienced specialists are unusual for bumblebees in that they have all reached different conclusions on the number of species present. Recent revisions based on skeletal morphology have concluded that there are from four to six species, while variation in colour pattern of the hair raised questions as to whether at least seven species might be present. Even more species are supported if we accept the recent move away from viewing species as morphotypes to viewing them instead as evolutionarily independent lineages (EILs) using data from genes. EILs are recognised here in practice from the gene coalescents that provide direct evidence for their evolutionary independence. We show from fitting both general mixed Yule/coalescent (GMYC) models and Poisson-tree-process (PTP) models to data for the mitochondrial COI gene that there is support for nine species in the subgenus Alpinobombus. Examination of the more slowly evolving nuclear PEPCK gene shows further support for a previously unrecognised taxon as a new species in northwestern North America. The three pairs of the most morphologically similar sister species are separated allopatrically and prevented from interbreeding by oceans. We also find that most of the species show multiple shared colour patterns, giving the appearance of mimicry among parts of the different species. However, reconstructing ancestral colour-pattern states shows that speciation is likely to have cut across widespread ancestral polymorphisms, without or largely without convergence. In the particular case of Alpinobombus, morphological, colour-pattern, and genetic groups show little agreement, which may help to explain the lack of agreement among previous taxonomic revisions.

Bumblebees, climate and glaciers across the Tibetan plateau (Apidae: Bombus Latreille)

The Tibetan plateau and its immediately surrounding mountains include the greatest hotspot of diversity worldwide for bumblebees, which are among the most important pollinators in temperate ecosystems. We make the first quantitative description of variation in the species composition of alpine social bumblebee faunas across the Tibetan plateau, for 44 species in 124 of the 307 one-degree grid cells. Data were compiled from field surveys, published sources and museum collections. Sampling effort could not be standardized across the region so our inferences have to be provisional. Faunal variation is described using detrended correspondence analysis (DCA); the faunal variation explained by climate variation is described using canonical correlation analysis (CCA); and the contribution of the climate data to the explanation is assessed using Procrustes analysis. Results show: (1) a particularly distinct group of endemic Himalayan faunas in the south; (2) a group of Tibetan interior faunas, with connections to faunas in the north-west in the Hindu Kush, Pamir and Tian Shan; and (3) a group of faunas in north-eastern Qinghai and Gansu, with connections to faunas to the north-east in Mongolia. The eastern and southern faunas in wetter habitats appear to be closer to equilibrium with climate factors, whereas some western faunas in more arid habitats appear further from equilibrium with the measured climate factors. One possibility is that these western faunas may depend on highly localized factors for mitigating the low precipitation over much of this region, and particularly on continuous summer streams with meltwater from distant permanent glaciers or high-ridge precipitation. Consequently, conservation threats to Tibetan bumblebees now include climate change causing loss of permanent streams in the west as well as the over-grazing documented in the east, threats that have not been major concerns for bumblebee conservation elsewhere.

Comparison of the colony development of two native bumblebee species Bombus ignitus and Bombus lucorum as candidates for commercial pollination in China

Summary Studies of the colony development of the Chinese bumble bees Bombus ignitus and Bombus lucorum found that there were four oviposition phases. The average number of workers produced per colony of B. ignitus and B. lucorum was 107 and 104 respectively, there being no significant difference between them (p>0.05). Colonies produced daughter queens in Phase 4 and the average number of new queens produced per colony of B. ignitus was smaller than that of B. lucorum (p<0.05). The proportion of B. ignitus and B. lucorum queens which established nests was on average 89% and 84% respectively (p>0.05). The average time to the emergence of the first workers in B. lucorum was longer than in B. ignitus, and this was significantly different (p<0.05), but the percentage of successful colony production of B. lucorum was lower than that of B. ignitus, and the number of workers which had emerged at above 30 days after first the oviposition in B. lucorum was more than in B. ignitus.

Newly discovered colour-pattern polymorphism of Bombus koreanus females (Hymenoptera: Apidae) demonstrated by DNA barcoding

Bombus (Megabombus) koreanus (Skorikov) is a long-tongued bumblebee that specialises in visiting deep flowers. To describe the distribution, colour-pattern variation and food plants of B. koreanus, we collected specimens and DNA cytochrome oxidase I (COI) barcodes were obtained. Bayesian phylogenetic analysis of barcodes for Megabombus species shows that B. koreanus is one of the more recently diverged species and the sister species to Bombus consobrinus. Our results show that specimens with previously unknown colour patterns also belong to B. koreanus. We describe nine different colour patterns for workers and three for queens, in which the hair of the thorax varies from black to orange-brown. However, there is a lack of covariation between COI and colour-pattern variation. B. koreanus has been recorded to visit 11 species of food plants showing that B. koreanus is polylectic. Our results demonstrate that COI barcoding is an effective method for studying closely related taxa and for recognising species with variable colour patterns.

BBCI: A new initiative to document Chinese bumble bees for pollination research

Paul Williams, Jiandong An, Jiaxing Huang and Jian Yao Department of Entomology, The Natural History Museum, London, SW7 5BD, UK. Key Laboratory for Insect-Pollinator Biology of the Ministry of Agriculture, Institute of Apiculture, Chinese Academy of Agricultural Sciences, Beijing 100093, PR China. Department of Entomology, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, PR China.

Extreme food-plant specialisation in Megabombus bumblebees as a product of long tongues combined with short nesting seasons.

Megabombus bumblebees have unusually long tongues and are generally more specialised than other bumblebees in their choice of food plants. The phylogeny of Megabombus bumblebees shows that speciation was concentrated in two periods. Speciation in the first period (ca 4.25–1.5 Ma) is associated with the late rise of the Hengduan Mountains at the eastern end of the Qinghai-Tibetan plateau. Speciation in the second period (1.2–0.3 Ma) is associated with climatic cooling in the northern forests. The most extreme food-specialist species belong to the second period, which may point to climate as a factor in specialisation. These extreme specialist species occur either in the far north (Bombus consobrinus), or at high elevations (Bombus gerstaeckeri), in situations where long tongues coincide with the shortest nesting seasons. Species with the longest tongues but occurring further south (even at high elevations) use a broader range of food plants.

Early-diverging bumblebees from across the roof of the world: the high-mountain subgenus Mendacibombus revised from species’ gene coalescents and morphology (Hymenoptera, Apidae)

The bumblebees of the subgenus Mendacibombus of the genus Bombus are the sister group to all other extant bumblebees and are unusual among bees for specialising in some of the highest elevation habitats with entomophilous plants on Earth. Most named taxa in this group (24 available names, from a total of 49 published names) were described originally from small differences in the colour pattern of the hair, many as parts (e.g. subspecies) of just one species. Subsequent taxonomic treatments recognised multiple species, but have described very few morphological characters, most of which are in the male genitalia. We examined 4413 specimens representing all of the named taxa from throughout the groups global range to describe variation in DNA, in skeletal morphology, and in the colour patterns of the hair. Using Bayesian inference of the phylogeny from an evolutionary model for the fast-evolving COI gene, and fitting either general mixed Yule/coalescent models or Poisson tree process models, we identify COI gene coalescents, which are expected to characterise species as evolutionarily independent lineages. None of the conditions most likely to compromise this interpretation (biased sampling, paralogy, introgression, heteroplasmy, incomplete lineage sorting) appears to be a substantial problem in this case. In an integrative analysis, we show that colour patterns are often variable within these groups and do not diagnose the same groups as we recognise from genes; in contrast, the groups recognised from gene coalescents can also be diagnosed from differences we identify in morphology. We infer that the 12 groups with coalescents in the COI gene that are corroborated by morphology constitute species, whereas many of these species are polymorphic in colour pattern. Lectotypes are designated for 15 taxa in order to reduce uncertainty in the identity and application of the names. We provide new morphological keys and distribution maps for the species. Then we use four genes (fast-evolving mitochondrial COI and 16S; and slower nuclear PEPCK and opsin) to obtain an absolute chronogram of phylogenetic relationships among the species. From published estimates that the most recent common ancestor of the subgenus Mendacibombus diverged from the other bumblebees at the beginning of the Oligocene, our results support the crown group of Mendacibombus as having diversified in the late Miocene, events that both appear to have been associated with periods of climate cooling. Relative conservatism in the alpine/subalpine climate niche of Mendacibombus, as compared with the much more diversified climate niches in the sister group of all other bumblebees, may have contributed to constraining the number of Mendacibombus species to just one twentieth of the total number of extant bumblebee species.