Abstract
BackgroundThe chromosome characteristics of the butterfly Bicyclus anynana, have received little attention, despite the scientific importance of this species. This study presents the characterization of chromosomes in this species by means of cytogenetic analysis and linkage mapping.Methodology/Principal FindingsPhysical genomic features in the butterfly B. anynana were examined by karyotype analysis and construction of a linkage map. Lepidoptera possess a female heterogametic W-Z sex chromosome system. The WZ-bivalent in pachytene oocytes of B. anynana consists of an abnormally small, heterochromatic W-chromosome with the Z-chromosome wrapped around it. Accordingly, the W-body in interphase nuclei is much smaller than usual in Lepidoptera. This suggests an intermediate stage in the process of secondary loss of the W-chromosome to a ZZ/Z sex determination system. Two nucleoli are present in the pachytene stage associated with an autosome and the WZ-bivalent respectively. Chromosome counts confirmed a haploid number of n = 28. Linkage mapping had to take account of absence of crossing-over in females, and of our use of a full-sib crossing design. We developed a new method to determine and exclude the non-recombinant uninformative female inherited component in offspring. The linkage map was constructed using a novel approach that uses exclusively JOINMAP-software for Lepidoptera linkage mapping. This approach simplifies the mapping procedure, avoids over-estimation of mapping distance and increases the reliability of relative marker positions. A total of 347 AFLP markers, 9 microsatellites and one single-copy nuclear gene covered all 28 chromosomes, with a mapping distance of 1354 cM. Conserved synteny of Tpi on the Z-chromosome in Lepidoptera was confirmed for B. anynana. The results are discussed in relation to other mapping studies in Lepidoptera.Conclusions/SignificanceThis study adds to the knowledge of chromosome structure and evolution of an intensively studied organism. On a broader scale it provides an insight in Lepidoptera sex chromosome evolution and it proposes a simpler and more reliable method of linkage mapping than used for Lepidoptera to date.
Highlights
The butterfly Bicyclus anynana (Nymphalidae, Satyrinae) is among the most extensively studied Lepidoptera species
Bivalents and male metaphase II chromosomes in male meiosis, and pachytene bivalents in female meiotic prophase I showed a haploid chromosome number of 28 for B. anynana in our stock from Malawi (Fig. 1A–C). This is consistent with the findings of [18] for B. anynana from Uganda and there is no evidence for geographical variation in chromosome numbers in this species
Female pachytene oocytes showed 27 fully-paired bivalents and a pair of sex chromosomes, consisting of a small heterochromatic W chromosome that has a circular arrangement and a Z chromosome that was wrapped around it in the majority of nuclei (Fig 1D); in some nuclei, the W chromosome was associated with a terminal segment of the Z chromosome (Fig. 1C) or less often with a central part of the Z chromosome (Fig. 1E) and formed a short thick rod or a body-like structure
Summary
The butterfly Bicyclus anynana (Nymphalidae, Satyrinae) is among the most extensively studied Lepidoptera species It has been established as an emerging model organism to address many evolutionary questions with a particular focus on genetic and environmental effects on wing pattern formation [1,2,3], and on life history evolution and ageing [4,5,6,7]. A haploid chromosome number of 28 was reported in B. anynana from Entebbe, Uganda [18], but given the geographical variability in Lepidoptera there is need for confirmation since the material used in the present study originates from Nkhata Bay in Malawi, about 1300 km to the south. This study presents the characterization of chromosomes in this species by means of cytogenetic analysis and linkage mapping
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