New Sex Chromosomes in Lake Victoria Cichlid Fishes (Cichlidae: Haplochromini)

African cichlid fishes harbor an extraordinary diversity of sex-chromosome systems. Within just one lineage, the tribe Haplochromini, at least 6 unique sex-chromosome systems have been identified. Here we focus on characterizing sex chromosomes in cichlids from the Lake Victoria basin. In Haplochromis chilotes, we identified a new ZW system associated with the white blotch color pattern, which shows substantial sequence differentiation over most of LG16, and is likely to be present in related species. In Haplochromis sauvagei, we found a coding polymorphism in amh that may be responsible for an XY system on LG23. In Pundamilia nyererei, we identified a feminizing effect of B chromosomes together with XY- and ZW-patterned differentiation on LG23. In Haplochromis latifasciatus, we identified a duplication of amh that may be present in other species of the Lake Victoria superflock. We further characterized the LG5-14 XY system in Astatotilapia burtoni and identified the oldest stratum on LG14. This species also showed ZW differentiation on LG2. Finally, we characterized an XY system on LG7 in Astatoreochromis alluaudi. This report brings the number of distinct sex-chromosome systems in haplochromine cichlids to at least 13, and highlights the dynamic evolution of sex determination and sex chromosomes in this young lineage.https://doi.org/10.3390/genes1305080

Patterns of genomic differentiation between two Lake Victoria cichlid species, Haplochromis pyrrhocephalus and H. sp. ‘macula’

Abstract Background The molecular basis of the incipient stage of speciation is still poorly understood. Cichlid fish species in Lake Victoria are a prime example of recent speciation events and a suitable system to study the adaptation and reproductive isolation of species. Results Here, we report the pattern of genomic differentiation between two Lake Victoria cichlid species collected in sympatry, Haplochromis pyrrhocephalus and H. sp. ‘macula,’ based on the pooled genome sequences of 20 individuals of each species. Despite their ecological differences, population genomics analyses demonstrate that the two species are very close to a single panmictic population due to extensive gene flow. However, we identified 21 highly differentiated short genomic regions with fixed nucleotide differences. At least 15 of these regions contained genes with predicted roles in adaptation and reproductive isolation, such as visual adaptation, circadian clock, developmental processes, adaptation to hypoxia, and sexual selection. The nonsynonymous fixed differences in one of these genes, LWS, were reported as substitutions causing shift in absorption spectra of LWS pigments. Fixed differences were found in the promoter regions of four other differentially expressed genes, indicating that these substitutions may alter gene expression levels. Conclusions These diverged short genomic regions may have contributed to the differentiation of two ecologically different species. Moreover, the origins of adaptive variants within the differentiated regions predate the geological formation of Lake Victoria; thus Lake Victoria cichlid species diversified via selection on standing genetic variation

Intraspecific sexual selection on a speciation trait, male coloration, in the Lake Victoria cichlid Pundamilia nyererei.

The haplochromine cichlids of Lake Victoria constitute a classical example of explosive speciation. Extensive intra- and interspecific variation in male nuptial coloration and female mating preferences, in the absence of postzygotic isolation between species, has inspired the hypothesis that sexual selection has been a driving force in the origin of this species flock. This hypothesis rests on the premise that the phenotypic traits that underlie behavioural reproductive isolation between sister species diverged under sexual selection within a species. We test this premise in a Lake Victoria cichlid, by using laboratory experiments and field observations. We report that a male colour trait, which has previously been shown to be important for behavioural reproductive isolation between this species and a close relative, is under directional sexual selection by female mate choice within this species. This is consistent with the hypothesis that female choice has driven the divergence in male coloration between the two species. We also find that male territoriality is vital for male reproductive success and that multiple mating by females is common

Maps and Frequencies of <i>LWS</i> Alleles

<div><p>(A) The study area in southern Lake Victoria. Arabic numerals indicate stations at which cichlids were collected. The Secchi disk water transparency (cm) at each station is shown in parentheses. The stations are: 1, Buyago Rocks; 2, Marumbi Island; 3, Matumbi Island; 4, Luanso Island; 5, Python (Nyamatala) Islands; 6, Kissenda Island; 7, Hippo Island; 8, Juma Island; 9, Bwiru Point; 10, Makobe Island; 11, Igombe Island; 12, Ruti Island; 13, Senga Point; 14, Sozihe Islands; 15, Namatembi Island; 16, Nyamatala (Nyameruguyu) Island; 17, Gabalema Islands; 18, north end of Luanso Bay. Where the local name differs from that used in previous publications, the local name is indicated in parenthesis.</p> <p>(B) A representation of the microhabitat distribution of the studied species by water depth and between, as opposed to outside, the rocky boulders. Photos show males of the blue morph in nuptial coloration. “Affected” and “Non-affected” indicate the species with the <i>LWS</i> allele frequencies that are strongly affected and not strongly affected by variation in water transparency, respectively.</p> <p>(C) <i>LWS</i> allele group frequencies in the populations of <i>N. greenwoodi/omnicaeruleus</i>.</p> <p>(D) <i>LWS</i> allele group frequencies in the populations of M. mbipi.</p> <p>(E) <i>LWS</i> allele group frequencies in the populations of N. rufocaudalis.</p> <p>(F) <i>LWS</i> allele group frequencies in the populations of P. pundamilia.</p> <p>In (B–E), Arabic numerals correspond to those in (A). The size of a pie indicates the number of haplotypes sequenced: N. greenwoodi: <i>n</i> = 58 at station 2; <i>n</i> = 10 at 3; <i>n</i> = 14 at 5; <i>n</i> = 10 at 7; <i>n</i> = 14 at 9; <i>n</i> = 22 at 11; <i>n</i> = 8 at 13; <i>n</i> = 8 at 14; <i>n</i> = 50 at 15, and <i>N. omnicaeruleus, n</i> = 40 at 10. M. mbipi: <i>n</i> = 36 at station 5; <i>n</i> = 32 at 7; <i>n</i> = 30 at 10; <i>n</i> = 10 at 11; <i>n</i> = 2 at 13. N. rufocaudalis: <i>n</i> = 42 at station 5; <i>n</i> = 16 at 6; <i>n</i> = 10 at 10; <i>n</i> = 10 at 16; <i>n</i> = 6 at 17; <i>n</i> = 4 at 18. P. pundamilia: <i>n</i> = 2 at station 1; <i>n</i> = 10 at 2; <i>n</i> = 4 at 3; <i>n</i> = 8 at 4; <i>n</i> = 18 at 5; <i>n</i> = 8 at 6; <i>n</i> = 6 at 8; <i>n</i> = 6 at 9; <i>n</i> = 10 at 10; <i>n</i> = 6 at 11; <i>n</i> = 8 at 12. The color of the sections of the pie indicates the frequency of allele groups L (red), M1 (yellow), M2 (green), H (blue), M3 (orange), P (blue-green), and other alleles (black). The amino acid differences among allele groups are shown for every species in the corresponding white panels.</p></div

Absorption Spectra of the LWS Pigments Evaluated by the Dark–Light Difference Spectra

<p>The LWS pigments were reconstituted from (A) H allele with A1 retinal, (B) L allele with A1 retinal, (C) H allele with A2 retinal, and (D) L allele with A2 retinal. The λ_max values are indicated with their standard errors.</p

Divergent selection on opsins drives incipient speciation in Lake Victoria cichlids. PLoS Biology 4:2244–51

Divergent natural selection acting on ecological traits, which also affect mate choice, is a key element of ecological speciation theory, but has not previously been demonstrated at the molecular gene level to our knowledge. Here we demonstrate parallel evolution in two cichlid genera under strong divergent selection in a gene that affects both. Strong divergent natural selection fixed opsin proteins with different predicted light absorbance properties at opposite ends of an environmental gradient. By expressing them and measuring absorbance, we show that the reciprocal fixation adapts populations to divergent light environments. The divergent evolution of the visual system coincides with divergence in male breeding coloration, consistent with incipient ecological by-product speciation

Speciation through sensory drive in cichlid fish

Theoretically, divergent selection on sensory systems can cause speciation through sensory drive. However, empirical evidence is rare and incomplete. Here we demonstrate sensory drive speciation within island populations of cichlid fish. We identify the ecological and molecular basis of divergent evolution in the cichlid visual system, demonstrate associated divergence in male colouration and female preferences, and show subsequent differentiation at neutral loci, indicating reproductive isolation. Evidence is replicated in several pairs of sympatric populations and species. Variation in the slope of the environmental gradients explains variation in the progress towards speciation: speciation occurs on all but the steepest gradients. This is the most complete demonstration so far of speciation through sensory drive without geographical isolation. Our results also provide a mechanistic explanation for the collapse of cichlid fish species diversity during the anthropogenic eutrophication of Lake Victoria