Population Genomics Provide Insights into the Evolution and Adaptation of the Eastern Honey Bee (Apis cerana)

Chen, Chao; Wang, Huihua; Liu, Zhiguang; Chen, Xiao; Tang, Jiao; Meng, Fanming; Shi, Wei

doi:10.1093/molbev/msy130

Cited by 73 publications

(102 citation statements)

References 72 publications

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“…We conducted a kinship assessment for each population using the program plink (Purcell et al, ) with the “‐‐genome” flag. As this calculation is not LD‐sensitive, we did LD‐based pruning using the same parameters as Chen et al () (–indep 50 5 1.1). We assessed population genetic structure across all populations using two different clustering programs, snmf (Frichot, Mathieu, Trouillon, Bouchard, & François, ) and admixture v 1.3.0 (Alexander, Novembre, & Lange, ) in addition to a principal component analysis (PCA) with the function “glPca” from the adegenet R package (Jombart, ).…”

Section: Methodsmentioning

confidence: 99%

“…Physiological and behavioural differences may also be involved in this local adaptation. In a recent study based on WGS, A. cerana populations sampled across China were found to have limited levels of population structure, with the highest levels of genome differentiation and lower genetic diversity observed in isolated mountain or island populations (Chen et al, ), indicating a greater degree of reproductive isolation. However, the molecular basis of the phenotypic differences exhibited by highland populations is unknown.…”

Section: Introductionmentioning

confidence: 99%

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The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

et al. 2019

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The eastern honey bee (Apis cerana) is of central importance for agriculture in Asia. It has adapted to a wide variety of environmental conditions across its native range in southern and eastern Asia, which includes high‐altitude regions. eastern honey bees inhabiting mountains differ morphologically from neighbouring lowland populations and may also exhibit differences in physiology and behaviour. We compared the genomes of 60 eastern honey bees collected from high and low altitudes in Yunnan and Gansu provinces, China, to infer their evolutionary history and to identify candidate genes that may underlie adaptation to high altitude. Using a combination of FST‐based statistics, long‐range haplotype tests and population branch statistics, we identified several regions of the genome that appear to have been under positive selection. These candidate regions were strongly enriched for coding sequences and had high haplotype homozygosity and increased divergence specifically in highland bee populations, suggesting they have been subjected to recent selection in high‐altitude habitats. Candidate loci in these genomic regions included genes related to reproduction and feeding behaviour in honey bees. Functional investigation of these candidate loci is necessary to fully understand the mechanisms of adaptation to high‐altitude habitats in the eastern honey bee.

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

et al. 2019

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“…And thirdly, the gut microbiota of A. mellifera harbored a much larger repertoire of enzymes related to polysaccharide breakdown. Thus, in the time since their last common ancestor, approximately 6 million years ago [20, 23], the gut bacterial communities of A. mellifera and A. cerana seem to have undergone substantial changes in composition, genomic diversity, and functionality, with likely consequences for the interaction with their hosts.…”

Section: Discussionmentioning

confidence: 99%

“…In the current study, we perform a comparative metagenomic analysis of the gut microbiota of two closely related species of honey bees, Apis mellifera and Apis cerana . Based on molecular data, their last common ancestor has been dated to approximately 6 million years ago [20–23], and previous 16S rRNA-based studies have shown that they harbor largely overlapping gut microbiota phylotypes (>97% 16S rRNA identity) [13]. With the exception of A. mellifera , all extant species of honey bees (genus Apis ) are confined to Asia, pointing towards an Asian origin of the Apis genus [21].…”

Section: Introductionmentioning

confidence: 99%

Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

Ellegaard¹,

Suenami

Miyazaki

et al. 2020

Preprint

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Most bacterial species encompass strains with vastly different gene content. Strain diversity in microbial communities is therefore considered to be of functional importance. Yet, little is known about the extent to which related microbial communities differ in diversity at this level and which underlying mechanisms may constrain and maintain strain-level diversity. Here, we used shotgun metagenomics to characterize and compare the gut microbiota of two honey bee species, Apis mellifera and Apis cerana, which have diverged about 6 mio years ago. While both host species are colonized by largely overlapping bacterial 16S rRNA phylotypes, we find that their communities are highly host-specific when analyzed with genomic resolution. Despite their similar ecology, A. mellifera displayed a much higher extent of strain-level diversity and functional gene content in the microbiota than A. cerana, per colony and per individual bee. In particular, the gene repertoire for polysaccharide degradation was massively expanded in the microbiota of A. mellifera relative to A. cerana. Bee management practices, divergent ecological adaptation, or habitat size may have contributed to the observed differences in microbiota composition of these two key pollinator species. Our results illustrate that the gut microbiota of closely related animal hosts can differ vastly in genomic diversity despite sharing similar levels of diversity at the 16S rRNA gene. This is likely to have consequences for gut microbiota functioning and host-symbiont interactions, highlighting the need for metagenomic studies to understand the ecology and evolution of microbial communities.

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“…These A. cerana populations differ in their nesting behaviour, such as the number of combs or even in their body size 86 . In China alone, A. cerana populations were shown to be as genetically divergent for more than 300,000 to 500,000 years (earlier than the recognized level of subspecies for A. mellifera) 112 . In addition to genetic differences between the hosts, 585 the climactic environments across Asia are highly variable and could result in local adaptation, though, as mentioned earlier, this did not prevent range expansions after switching hosts (Figure 1) 79,81 and may remain undetected.…”

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confidence: 99%

Divergent selection following speciation in two ectoparasitic honey bee mites

Techer

Rane

et al. 2019

Preprint

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31Multispecies host-parasite evolution is common, but how parasites evolve after speciating 32 remains poorly understood. Shared evolutionary history and physiology may propel species 33 along similar evolutionary trajectories whereas pursuing different strategies can reduce 34 competition. We test these scenarios in the economically important association between honey 35 bees and ectoparasitic mites by sequencing the genomes of the sister mite species Varroa 36 destructor and Varroa jacobsoni. These genomes were closely related, with 99.7% sequence 37 identity. Among the 9,628 orthologous genes, 4.8% showed signs of positive selection in at least 38 one species. Divergent selective trajectories were discovered in conserved chemosensory gene 39 families (IGR, SNMP), and Halloween genes (CYP) involved in moulting and reproduction. 40 However, there was little overlap in these gene sets and associated GO terms, indicating 41 different selective regimes operating on each of the parasites. Based on our findings, we 42 suggest that species-specific strategies may be needed to combat evolving parasite 43 communities. 45Interactions between hosts and parasites shape biodiversity by driving coevolutionary 46 arms races and by regulating populations over ecological timescales. Parasitism is a remarkably 47 109 41 and linking oogenesis initiation or failure to parasitic reduced metabolism and host defense 110 44,45 . 111Here, we ask how both mite species have arrived at this tolerance equilibrium in A. 112 ceranadid they follow similar or different evolutionary paths? On one hand, the two species 113 naturally occur in parapatry ( Figure 1B), which is expected to result from divergent local 114 adaptation with the distribution of different A. cerana lineages 46,47 . In actuality, what drives the 115 parapatric distribution is unclear. V. destructor, which was historically absent from Southeast 116 Asia, now occurs there on its novel host A. mellifera in sympatry with V. jacobsoni, which does 117 not parasitize A. mellifera in this region ( Figure 1C). Thus, it is possible that the current 118 geographical distribution resulted from secondary contact following allopatric speciation. This 119 view is further supported by the fact that both species have the genetic capacity to shift to A. 120 mellifera as a novel host, suggesting a level of physiological similarity. We tested these 121 alternative hypotheses (parallel vs. divergent evolution) by generating high-quality hybrid de 122 novo genome assembly of both species and examining them for signatures of adaptive 123 evolution. We also compared them to the recently published genome of a distantly related 124 ectoparasitic mite Tropilaelaps mercedesae, to see whether the patterns appear universal at 125 different timescales. 126 127 128 129 Figure 1: V. destructor and V. jacobsoni are morphologically similar sister species originally parasitizing 130 the eastern honey bee (A. cerana). These species were recognized upon the basis of quantitative 131 morphometric an...

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Population Genomics Provide Insights into the Evolution and Adaptation of the Eastern Honey Bee (Apis cerana)

Cited by 73 publications

References 72 publications

The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

The genomic basis of adaptation to high‐altitude habitats in the eastern honey bee (Apis cerana)

Vast differences in strain-level diversity in the gut microbiota of two closely related honey bee species

Divergent selection following speciation in two ectoparasitic honey bee mites

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