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Comparative genomics suggests local adaptations in the invasive small hive beetle

ABSTRACT: Abstract Invasive species are a major driver of ecological and environmental changes that affect human health, food security, and natural biodiversity. The success and impact of biological invasions depend on adaptations to novel abiotic and biotic selective pressures. However, the molecular mechanisms underlying adaptations in invasive parasitic species are inadequately understood. Small hive beetles, Aethina tumida, are parasites of bee nests. Originally endemic to sub‐Saharan Africa, they are now found nearly globally. Here, we investigated the molecular bases of the adaptations to novel environments underlying their invasion routes. Genomes of historic and recent adults A. tumida from both the endemic and introduced ranges were compared. Analysis of gene–environment association identified 3049 candidate loci located in 874 genes. Functional annotation showed a significant bias toward genes linked to growth and reproduction. One of the genes from the apoptosis pathway encodes an “ecdysone‐related protein,” which is a crucial regulator in controlling body size in response to environmental cues for holometabolous insects during cell death and renewal. Genes whose proteins regulate organ size, ovary activation, and oviposition were also detected. Functions of these enriched pathways parallel behavioral differences between introduced and native A. tumida populations, which may reflect patterns of local adaptation. The results considerably improve our understanding of the underlying mechanisms and ecological factors driving adaptations of invasive species. Deep functional investigation of these identified loci will help clarify the mechanisms of local adaptation in A. tumida. Small hive beetles, Aethina tumida, invasive parasites of pollinating bees have recently invaded multiple continents, across a wide range of climates. The molecular mechanisms underlying the adaptation of this invasive beetle remain poorly understood. Here, the identification of genetic basis, analyses of gene ontology, and pathway enrichment of identified genes provide a mechanistic understanding of a biological invasion.

SUBMITTER: Liu Y

PROVIDER: S-EPMC8601931 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Pneumocystis species are fungal parasites of mammal lungs showing host specificity. Pneumocystis jirovecii colonizes humans and causes severe pneumonia in immunosuppressed individuals. In the absence of in vitro cultures, the life cycle of these fungi remains poorly known. Sexual reproduction probably occurs, but the system of this process and the mating type (MAT) genes involved are not characterized. In the present study, we used comparative genomics to investigate the issue in P. jirovecii and Pneumocystis carinii, the species infecting rats, as well as in their relative Taphrina deformans. We searched sex-related genes using 103 sequences from the relative Schizosaccharomyces pombe as queries. Genes homologous to several sex-related role categories were identified in all species investigated, further supporting sexuality in these organisms. Extensive in silico searches identified only three putative MAT genes in each species investigated (matMc, matMi, and matPi). In P. jirovecii, these genes clustered on the same contig, proving their contiguity in the genome. This organization seems compatible neither with heterothallism, because two different MAT loci on separate DNA molecules would have been detected, nor with secondary homothallism, because the latter involves generally more MAT genes. Consistently, we did not detect cis-acting sequences for mating type switching in secondary homothallism, and PCR revealed identical MAT genes in P. jirovecii isolates from six patients. A strong synteny of the genomic region surrounding the putative MAT genes exists between the two Pneumocystis species. Our results suggest the hypothesis that primary homothallism is the system of reproduction of Pneumocystis species and T. deformans. Sexual reproduction among fungi can involve a single partner (homothallism) or two compatible partners (heterothallism). We investigated the issue in three pathogenic fungal relatives: Pneumocystis jirovecii, which causes severe pneumonia in immunocompromised humans; Pneumocystis carinii, which infects rats; and the plant pathogen Taphrina deformans. The nature, the number, and the organization within the genome of the genes involved in sexual reproduction were determined. The three species appeared to harbor a single genomic region gathering only three genes involved in sexual differentiation, an organization which is compatible with sexual reproduction involving a single partner. These findings illuminate the strategy adopted by fungal pathogens to infect their hosts.

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Comparative genomics suggests local adaptations in the invasive small hive beetle

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