The genome of the Trinidadian guppy, Poecilia reticulata, and variation in the Guanapo population

For over a century, the live bearing guppy, Poecilia reticulata, has been used to study sexual selection as well as local adaptation. Natural guppy populations differ in many traits that are of intuitively adaptive significance such as ornamentation, age at maturity, brood size and body shape. Water depth, light supply, food resources and predation regime shape these traits, and barrier waterfalls often separate contrasting environments in the same river. We have assembled and annotated the genome of an inbred single female from a high-preda- tion site in the Guanapo drainage. The final assembly comprises 731.6 Mb with a scaffold N50 of 5.3 MB. Scaffolds were mapped to linkage groups, placing 95% of the genome assembly on the 22 autosomes and the X-chromosome. To investigate genetic variation in the population used for the genome assembly, we sequenced 10 wild caught male individu- als. The identified 5 million SNPs correspond to an average nucleotide diversity (π) of 0.0025. The genome assembly and SNP map provide a rich resource for investigating adap- tation to different predation regimes. In addition, comparisons with the genomes of other Poeciliid species, which differ greatly in mechanisms of sex determination and maternal resource allocation, as well as comparisons to other teleost genera can begin to reveal how live bearing evolved in teleost fish

Improved reference genome uncovers novel sex-linked regions in the Guppy (Poecilia reticulata)

This is the author accepted manuscript. The final version is available on open access from Oxford University Press via the DOI in this recordData availability: Population genomics data are available on ENA: Study: PRJEB10680 PCR-free data are available on ENA: Study PRJEB36450 Genome assembly is available on ENA ID: PRJEB36704; ERP119926 All scripts and pipelines are available on github: https://github.com/bfrasercommits/guppy_genomeTheory predicts that the sexes can achieve greater fitness if loci with sexually antagonistic polymorphisms become linked to the sex determining loci, and this can favour the spread of reduced recombination around sex determining regions. Given that sex-linked regions are frequently repetitive and highly heterozygous, few complete Y chromosome assemblies are available to test these ideas. The guppy system (Poecilia reticulata) has long been invoked as an example of sex chromosome formation resulting from sexual conflict. Early genetics studies revealed that male colour patterning genes are mostly but not entirely Y-linked, and that X-linkage may be most common in low predation populations. More recent population genomic studies of guppies have reached varying conclusions about the size and placement of the Y-linked region. However, this previous work used a reference genome assembled from short-read sequences from a female guppy. Here, we present a new guppy reference genome assembly from a male, using long-read PacBio single-molecule real-time sequencing (SMRT) and chromosome contact information. Our new assembly sequences across repeat- and GC-rich regions and thus closes gaps and corrects mis-assemblies found in the short-read female-derived guppy genome. Using this improved reference genome, we then employed broad population sampling to detect sex differences across the genome. We identified two small regions that showed consistent male-specific signals. Moreover, our results help reconcile the contradictory conclusions put forth by past population genomic studies of the guppy sex chromosome. Our results are consistent with a small Y-specific region and rare recombination in male guppies.Max Planck SocietyEuropean Research Council (ERC)Natural Environment Research Council (NERC

The colorful sex chromosomes of teleost fish

Teleost fish provide some of the most intriguing examples of sexually dimorphic coloration, which is often advantageous for only one of the sexes. Mapping studies demonstrated that the genetic loci underlying such color patterns are frequently in tight linkage to the sex-determining locus of a species, ensuring sex-specific expression of the corresponding trait. Several genes affecting color synthesis and pigment cell development have been previously described, but the color loci on the sex chromosomes have mostly remained elusive as yet. Here, we summarize the current knowledge about the genetics of such color loci in teleosts, mainly from studies on poeciliids and cichlids. Further studies on these color loci will certainly provide important insights into the evolution of sex chromosomes

Multiple pigment cell types contribute to the black, blue, and orange ornaments of male guppies (Poecilia reticulata).

The fitness of male guppies (Poecilia reticulata) highly depends on the size and number of their black, blue, and orange ornaments. Recently, progress has been made regarding the genetic mechanisms underlying male guppy pigment pattern formation, but we still know little about the pigment cell organization within these ornaments. Here, we investigate the pigment cell distribution within the black, blue, and orange trunk spots and selected fin color patterns of guppy males from three genetically divergent strains using transmission electron microscopy. We identified three types of pigment cells and found that at least two of these contribute to each color trait. Further, two pigment cell layers, one in the dermis and the other in the hypodermis, contribute to each trunk spot. The pigment cell organization within the black and orange trunk spots was similar between strains. The presence of iridophores in each of the investigated color traits is consistent with a key role for this pigment cell type in guppy color pattern formation

Transcriptome assemblies for studying sex-biased gene expression in the guppy, Poecilia reticulata

BACKGROUND: Sexually dimorphic phenotypes are generally associated with differential gene expression between the sexes. The study of molecular evolution and genomic location of these differentially expressed, or sex-biased, genes is important for understanding inter-sexual divergence under sex-specific selection pressures. Teleost fish provide a unique opportunity to examine this divergence in the presence of variable sex-determination mechanisms of recent origin. The guppy, Poecilia reticulata, displays sexual dimorphism in size, ornaments, and behavior, traits shaped by natural and sexual selection in the wild. RESULTS: To gain insight into molecular mechanisms underlying the guppy’s sexual dimorphism, we assembled a reference transcriptome combining genome-independent as well as genome-guided assemblies and analyzed sex-biased gene expression between different tissues of adult male and female guppies. We found tissue-associated sex-biased expression of genes related to pigmentation, signal transduction, and spermatogenesis in males; and growth, cell-division, extra-cellular matrix organization, nutrient transport, and folliculogenesis in females. While most sex-biased genes were randomly distributed across linkage groups, we observed accumulation of ovary-biased genes on the sex linkage group, LG12. Both testis-biased and ovary-biased genes showed a significantly higher rate of non-synonymous to synonymous substitutions (d(N)/d(S)) compared to unbiased genes. However, in somatic tissues only female-biased genes, including those co-expressed in multiple tissues, showed elevated ratios of non-synonymous substitutions. CONCLUSIONS: Our work identifies a set of annotated gene products that are candidate factors affecting sexual dimorphism in guppies. The differential genomic distribution of gonad-biased genes provides evidence for sex-specific selection pressures acting on the nascent sex chromosomes of the guppy. The elevated rates of evolution of testis-biased and female-biased genes indicate differing evolution under distinct selection pressures on the reproductive versus non-reproductive tissues. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/1471-2164-15-400) contains supplementary material, which is available to authorized users

Ultrastructure of fin color patterns.

<p>(A,D,F) Detail images of regions boxed in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g002" target="_blank">Figure 2A, 2C, and 2E</a> taken under incident light conditions. (D) and (F) are from the individual shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g002" target="_blank">Figure 2E and 2C</a>, respectively. (A) is from a Cumaná male different from the one shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g002" target="_blank">Figure 2A</a>. (B,C,E,G) TEM images. (A) Cumaná orange-black margin of tail fin (trait 4). The ultrastructure of the orange part is shown in (B) and (C). (D) Maculatus dorsal fin ornaments (trait 9). The ultrastructure of the whitish part is shown in (E). (F) Quare6 tail fin pattern (trait 5). The ultrastructure of the whitish area is shown in (G). For abbreviations see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g003" target="_blank">Figures 3</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g004" target="_blank">4</a>. Individual from which image (C) was taken was post-fixed with osmium tetroxide. Scale bars: (A,D,F) 500 µm; (B) 5 µm; (C,G) 1 µm; (E) 2 µm.</p

Phenotypes of male Cumaná, Quare6, and Maculatus guppies.

<p>(A,C,E) Lateral aspects of adult males taken under incident light conditions. White rectangles indicate details enlarged in (B,D,F) and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g006" target="_blank">Figures 6</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g007" target="_blank">7</a>. Traits are labeled with numbers according to their appearance in the text: 1, Cumaná black and orange ornaments on the dorsal fin; 2, Cumaná blue iridescent spot; 3, Cumaná ventral black margin of the caudal peduncle; 4, Cumaná orange-black lining of the tail fin; 5, Quare6 tail fin color pattern; 6, central black spot; 7, central orange spot; 8, Quare6 posterior black spot on caudal peduncle; 9, Maculatus black spot and whitish ornaments on the dorsal fin. We investigated the ultrastructure of traits 2, 4 (orange part), 5, 6, 7, 8, and 9 (whitish part). Scale bars: (A,C,E) 0.5 cm; (B,D,F) 500 µm.</p

Pigment cell types of the guppy.

<p>Xanthophores (X), melanophores (M) and iridophores (I) on the dorsal side of a guppy female shown under incident light. Leucophores could not be identified. Scale bar: 200 µm.</p

Ultrastructure of Cumaná blue spot.

<p>(A,B) TEM images of Cumaná blue spot. An image of the blue spot taken under incident light conditions is shown in <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g002" target="_blank">Figure 2B</a> (trait 2). Dermal iridophores and hypodermal iridophores and melanophores contribute to the spot. The epidermis was detached during sample preparation in (A). D, dermis; H, hypodermis; MU, muscle; S, scale; SP, stratum spongiosum of dermis. For other abbreviations see <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0085647#pone-0085647-g003" target="_blank">Figure 3</a>. Individual from which image (A) was taken was post-fixed with osmium tetroxide. Scale bars: 5 µm.</p