Sex without sex chromosomes: genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod <i>Tigriopus californicus</i>

Alexander, Heather J.; Richardson, Jean M. L.; Edmands, Suzanne; Anholt, Bradley R.

doi:10.1111/jeb.12743

Cited by 43 publications

(58 citation statements)

References 69 publications

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“…This evolution should, however, be highly dependent on environmental and developmental conditions (Van Dooren & Leimar, 2003; Van Doorn, 2014). Hence, it is likely that sex determination could take different directions in different populations and that the main sex determining loci may be distinct from one population to the other (see, e.g., Alexander, Richardson, Edmands, & Anholt, 2015 and references therein). The nonadditive component observed here could be supportive of synergistic effects of different sex factors developed in different populations from a common ancestral polygenic system.…”

Section: Discussionmentioning

confidence: 99%

“…(2005). Situations in which polygenic sex determination mediated by mtDNA effects could generate striking changes in sex ratio among distinct hybrid crosses have just begun to be explored in T. californicus (Alexander et al., 2015; Foley, Rose, Rundle, Leong, & Edmands, 2013) and in freshwater fish species ( Cottus sp . ; Cheng, Czypionka, & Nolte, 2013).…”

Section: Discussionmentioning

confidence: 99%

“…Because of pleiotropy (see above), asymmetric selection could act on early survival and favor sex determination of the individuals ♂ WEM × ♀ NAT cross as males as suggested by Lemaire et al (2005). Situations in which polygenic sex determination mediated by mtDNA effects could generate striking changes in sex ratio among distinct hybrid crosses have just begun to be explored in T. californicus (Alexander et al, 2015;Foley, Rose, Rundle, Leong, & Edmands, 2013) and in freshwater fish species (Cottus sp. ; Cheng, Czypionka, & Nolte, 2013).…”

Section: Relative Performances Of Reciprocal Nat × Wem Crossesmentioning

confidence: 99%

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Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

Guinand

Vandeputte

Dupont‐Nivet³

et al. 2017

Ecology and Evolution

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Describing and explaining the geographic within‐species variation in phenotypes (“phenogeography”) in the sea over a species distribution range is central to our understanding of a variety of eco‐evolutionary topics. However, phenogeographic studies that have a large potential to investigate adaptive variation are overcome by phylogeographic studies, still mainly focusing on neutral markers. How genotypic and phenotypic data could covary over large geographic scales remains poorly understood in marine species. We crossed 75 noninbred sires (five origins) and 26 dams (two origins; each side of a hybrid zone) in a factorial diallel cross in order to investigate geographic variation for early survival and sex ratio in the metapopulation of the European sea bass (Dicentrarchus labrax), a highly prized marine fish species. Full‐sib families (N = 1,950) were produced and reared in a common environment. Parentage assignment of 7,200 individuals was performed with seven microsatellite markers. Generalized linear models showed significant additive effects for both traits and pleiotropy between traits. A significant nonadditive genetic effect was detected. Different expression of traits and distinct relative performances were found for reciprocal crosses involving populations located on each side of the main hybrid zone located at the Almeria‐Oran front, illustrating asymmetric reproductive isolation. The poor fitness performance observed for the Western Mediterranean population of sea bass is discussed as it represents the main source of seed hatchery production, but also because it potentially illustrates nonadaptive introgression and maladaptation.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Relative Performances Of Reciprocal Nat × Wem Crossesmentioning

confidence: 99%

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Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

Guinand

Vandeputte

Dupont‐Nivet³

et al. 2017

Ecology and Evolution

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“…In polygenic sex determination systems, multiple, independently segregating sex determination alleles interact to determine sex within a species [3]. Historically, examples of polygenic sex determination were considered anomalous or evolutionarily transitory; however, with broader surveys and readily available genomic tools, polygenic sex determination has been identified in multiple animal taxa, including fish, mammals, insects, and copepods [3, 19], suggesting that polygenic sex determination is a common and stable evolutionary strategy.…”

Section: Introductionmentioning

confidence: 99%

Polygenic sex determination in the cichlid fish Astatotilapia burtoni

et al. 2016

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BackgroundThe East African riverine cichlid species Astatotilapia burtoni serves as an important laboratory model for sexually dimorphic physiology and behavior, and also serves as an outgroup species for the explosive adaptive radiations of cichlid species in Lake Malawi and Lake Victoria. An astounding diversity of genetic sex determination systems have been revealed within the adaptive radiation of East African cichlids thus far, including polygenic sex determination systems involving the epistatic interaction of multiple, independently segregating sex determination alleles. However, sex determination has remained unmapped in A. burtoni. Here we present mapping results supporting the presence of multiple, novel sex determination alleles, and thus the presence of polygenic sex determination in A. burtoni.ResultsUsing mapping in small families in conjunction with restriction-site associated DNA sequencing strategies, we identify associations with sex at loci on linkage group 13 and linkage group 5–14. Inheritance patterns support an XY sex determination system on linkage group 5–14 (a chromosome fusion relative to other cichlids studied), and an XYW system on linkage group 13, and these associations are replicated in multiple families. Additionally, combining our genetic data with comparative genomic analysis identifies another fusion that is unassociated with sex, with linkage group 8–24 and linkage group 16–21 fused in A. burtoni relative to other East African cichlid species.ConclusionsWe identify genetic signals supporting the presence of three previously unidentified sex determination alleles at two loci in the species A. burtoni, strongly supporting the presence of polygenic sex determination system in the species. These results provide a foundation for future mapping of multiple sex determination genes and their interactions. A better understanding of sex determination in A. burtoni provides important context for their use in behavioral studies, as well as studies of the evolution of genetic sex determination and sexual conflicts in East African cichlids.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-3177-1) contains supplementary material, which is available to authorized users.

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“…Strong support for the importance of mito-nuclear DMI has been found in the copepod Tigriopus californicus, a species that lacks sex chromosomes. This copepod, which lives in high intertidal pools on the west coast of North America, has polygenic sex determination with several unlinked factors contributing to sex determination (Voordouw and Anholt 2002;Alexander et al 2014Alexander et al , 2015. Tigriopus californicus populations occupy rocky pools on headlands that are often isolated from other headlands by long stretches of sandy beach.…”

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confidence: 99%

Genomic scans reveal multiple mito‐nuclear incompatibilities in population crosses of the copepod Tigriopus californicus

2019

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The evolution of intrinsic postzygotic isolation can be explained by the accumulation of Dobzhansky‐Muller incompatibilities (DMI). Asymmetries in the levels of hybrid inviability and hybrid sterility are commonly observed between reciprocal crosses, a pattern that can result from the involvement of uniparentally inherited factors. The mitochondrial genome is one such factor that appears to participate in DMI in some crosses but the frequency of its involvement versus biparentally inherited factors is unclear. Here we assess the relative importance of incompatibilities between nuclear factors (nuclear‐nuclear) versus those between mitochondrial and nuclear factors (mito‐nuclear) in a species that lacks sex chromosomes. We used a Pool‐seq approach to survey three crosses among genetically divergent populations of the copepod, Tigriopus californicus, for regions of the genome that are affected by hybrid inviability. Results from reciprocal crosses suggest that mito‐nuclear incompatibilities are more common than nuclear‐nuclear incompatibilities overall. These results suggest that in the presence of very high levels of nucleotide divergence between mtDNA haplotypes, mito‐nuclear incompatibilities can be important for the evolution of intrinsic postzygotic isolation. This is particularly interesting considering this species lacks sex chromosomes, which have been shown to harbor a particularly high number of nuclear‐nuclear DMI in several other species.

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Sex without sex chromosomes: genetic architecture of multiple loci independently segregating to determine sex ratios in the copepod Tigriopus californicus

Cited by 43 publications

References 69 publications

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

Metapopulation patterns of additive and nonadditive genetic variance in the sea bass (Dicentrarchus labrax)

Polygenic sex determination in the cichlid fish Astatotilapia burtoni

Genomic scans reveal multiple mito‐nuclear incompatibilities in population crosses of the copepod Tigriopus californicus

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