We have reported here a dense genetic linkage map of the guppy, which provides a basis for further genetic and molecular studies of sex linkage of male-advantageous genes, as well as natural variation of quantitative adaptive traits. The synteny information facilitates selection of candidate genes during fine mapping of QTL, since the guppy genome has not yet been sequenced.
Based on crosses involving ornamental guppy strains, quite variable lengths of the genetic map had been estimated (Khoo et al. 2003
; Watanabe et al. 2005
; Shen et al. 2007
). Our genetic map has a length of 899
cM, which is shorter compared with that of the medaka at 1354
cM (Naruse et al. 2000
), or even the closely related Xiphophorus
cM (Kazianis et al. 2004a
). Both species have 24 chromosomes compared with a haploid set of 23 in guppies and marginally higher estimated genomic DNA content (Cimino 1974
; Lamatsch et al. 2000
). Owing to the absence of an EST-linked map for the platyfish genome, we could not compare the synteny between guppy and platyfish genomes. In a comparative study with common microsatellite markers, the guppy was also found to have lower rates of recombination than Xiphophorus
, which is in the same family as the guppy (Brummell et al. 2006
). An explanation for the relatively short genetic length of the guppy map could be sequence inversions between the Cumaná and Quare populations, due to significant divergence (Alexander & Breden 2004
), which might result in reduced recombination frequency.
We have tested microsatellite markers from the sex chromosomes of platyfish, in addition to a set of selected candidate genes from the sex chromosome, but did not find any evidence of its sex linkage in the guppy (data not shown). Although from the present data, it seems likely that the sex-determining loci in platyfish and guppy are not homologous, we cannot prove it until we have additional markers from the diverged gonosomal region of guppy sex chromosomes, and more gene-linked markers from the sex chromosome of platyfish.
The differentiated region of the sex chromosome is likely to consist of expanded heterochromatin-rich sequences. Hence, due to the uncertain gap between the last mapped markers and the Sex locus, we have not included it in genome length estimates. Several additional markers that were placed with confidence on an LG, but could not be assigned to their accurate position (see table 6 in the electronic supplementary material), may add to the total genetic length when correctly positioned on the map. Therefore, the present calculated length could be a slight underestimate.
The multiple QTL mapped in this work affect traits that contribute to phenotypic variation of males in the two mapping populations. Several QTL were located on LG12, indicating that loci responsible for visible polymorphism in size, shape and colour patterns are enriched on the sex chromosome. This is in agreement with the previous knowledge of physical linkage of major colour pattern loci to sex chromosomes in the guppy (Winge 1927
; Winge & Ditlevsen 1947
; Haskins et al. 1970
; Brooks & Endler 2001a
; Lindholm & Breden 2002
). We do not believe that the enrichment for QTL reflects exceptional gene density on the sex chromosome, based on the extensive conserved synteny of the major portion of the guppy sex chromosome with an autosome of medaka.
While we do not yet have any markers from the Y-specific segment, due to the suppressed recombination between X and Y chromosomes, the reduced recombination facilitates the identification of QTL mapping to the sex LG. Unfortunately, for the same reason, it is difficult to resolve the precise locations of the sex-linked QTL. Based on the visual analysis of their segregation, we can predict certain Cumaná-derived alleles affecting quantitative colour traits (1, 2, 3 and 9 in b) to be in tight linkage with the Sex locus. Not all of these mapped to the expected region in the present QTL analysis, due to the absence of Y-linked markers.
The multiple genes detected for most of the traits mapped in this study probably reflect the complex nature of the traits, and indicate that their final expression may require a range of biological pathways and involve products of many genes. Furthermore, there will undoubtedly be additional loci, as a single mapping cross does not generally segregate all of the quantitative loci affecting any given trait (Mackay 1996
The MQM mapping results for selected shape traits and for areas of multiple colour traits suggest that multiple QTL of minor effect (lower LOD scores) contribute to each colour trait, while fewer large effect QTL with higher LOD scores may explain the selected shape traits.
In summary, the guppy genetic map will allow efficient use of the extensive genomic information available for several reference teleost fishes. In the long term, it will help to further our understanding of the genetic basis of adaptive evolution in this species and to explore the processes governing the evolution of genomes.