Abstract

Two microsporidians are known to infect honey bees: Nosema apis and Nosema ceranae. Whereas population genetics data for the latter have been released in the last few years, such information is still missing for N. apis. Here we analyze the patterns of nucleotide polymorphism at three single-copy loci (PTP2, PTP3 and RPB1) in a collection of Apis mellifera isolates from all over the world, naturally infected either with N. apis (N = 22) or N. ceranae (N = 23), to provide new insights into the genetic diversity, demography and evolution of N. apis, as well as to compare them with evidence from N. ceranae. Neutral variation in N. apis and N. ceranae is of the order of 1%. This amount of diversity suggests that there is no substantial differentiation between the genetic content of the two nuclei present in these parasites, and evidence for genetic recombination provides a putative mechanism for the flow of genetic information between chromosomes. The analysis of the frequency spectrum of neutral variants reveals a significant surplus of low frequency variants, particularly in N. ceranae, and suggests that the populations of the two pathogens are not in mutation-drift equilibrium and that they have experienced a population expansion. Most of the variation in both species occurs within honey bee colonies (between 62%-90% of the total genetic variance), although in N. apis there is evidence for differentiation between parasites isolated from distinct A. mellifera lineages (20%-34% of the total variance), specifically between those collected from lineages A and C (or M). This scenario is consistent with a long-term host-parasite relationship and contrasts with the lack of differentiation observed among host-lineages in N. ceranae (< 4% of the variance), which suggests that the spread of this emergent pathogen throughout the A. mellifera worldwide population is a recent event.

Highlights

  • The genus Nosema (Fungi, Microsporidia, Dihaplophasea, Dissociodihaplophasida Nosematidae; Nägeli, 1857) contains over eighty species [1,2] typically found in arthropods

  • We report a population genetic analysis conducted to address questions that are central to our understanding of the recent evolutionary history of N. apis, such as: what are the levels of genetic variation of this parasite? Is there any genetic evidence for a long-term association between N. apis and A. mellifera? Is the N. apis population panmictic or is there any sign of geographical structure? With this aim, the sequences of three single copy genes were studied in a collection of N. apis and N. ceranae isolates obtained from A. mellifera colonies from all over the world

  • The genetic variability of N. apis samples was initially assessed at PTP2, PTP3 and RPB1 in seven naturally infected A. mellifera colonies from Algeria, Argentina, Canada, Slovenia, Spain (N = 2) and Turkey

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Summary

Introduction

The genus Nosema (Fungi, Microsporidia, Dihaplophasea, Dissociodihaplophasida Nosematidae; Nägeli, 1857) contains over eighty species [1,2] typically found in arthropods. N. apis Zander, 1909 is a globally distributed pathogen that was identified in this host more than a hundred years ago [3], whereas N. ceranae was described at the end of the twentieth century [4] This latter species, initially discovered in the Asian honey bee Apis cerana [4], was recently proved to infect A. mellifera [5,6], and since it has been found worldwide in this new host [7,8,9,10,11], as well as in several other Apis [12,13] and Bombus species [14,15]. This effect, whose potential relationship with the large scale depopulation phenomenon is still matter of debate ([24,28], or [29,30] for a different point of view), is much more dramatic in Mediterranean countries, especially in Spain, where climatic conditions and/or beekeeping practices seem to increase the impact of N. ceranae on honey bee colonies reviewed in [31]

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