Development and evolution of insect polyphenisms: novel insights through the study of sex determination mechanisms

Moczek, Armin P.; Kijimoto, Teiya

doi:10.1016/j.cois.2014.05.004

Cited by 11 publications

(14 citation statements)

References 33 publications

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“…Phenotypic plasticity has been described in ecologically relevant traits such as leg length in Caribbean Anolis lizards (Losos et al . ), horn length in horned beetles (Emlen ; Moczek & Kijimoto ), castes in Hymenopterans (Cahan et al . ), body colour in spiny‐legged spiders (Brewer et al .…”

Section: Phenotypic Plasticity's Effect On Evolution and Speciationmentioning

confidence: 99%

“…Contrasting this view, plasticity in key ecological traits has often been found in taxa that are well known for their high rates of evolution and phenotypic diversification (Pfennig & McGee 2010). Phenotypic plasticity has been described in ecologically relevant traits such as leg length in Caribbean Anolis lizards (Losos et al 2000), horn length in horned beetles (Emlen 1994;Moczek & Kijimoto 2014), castes in Hymenopterans (Cahan et al 2004), body colour in spiny-legged spiders (Brewer et al 2015), feeding ecology and life history decisions in nematodes (Gutteling et al 2007;Serobyan et al 2013), body shape and jaw size in Oceanic sticklebacks (Wund et al 2008;Foster et al 2015;Mazzarella et al 2015) and pharyngeal jaw shape and dentition in cichlids (Box 3: Plasticity in cichlids) (e.g. Greenwood 1964;Meyer 1993b;Muschick et al 2012).…”

Section: Phenotypic Plasticity's Effect On Evolution and Speciationmentioning

confidence: 99%

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How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

2016

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There is increasing evidence that phenotypic plasticity can promote population divergence by facilitating phenotypic diversification and, eventually, genetic divergence. When a 'plastic' population colonizes a new habitat, it has the possibility to occupy multiple niches by expressing several distinct phenotypes. These initially reflect the population's plastic range but may later become genetically fixed by selection via the process of 'genetic assimilation' (GA). Through this process multiple specialized sister lineages can arise that share a common plastic ancestor - the 'flexible stem'. Here, we review possible molecular mechanisms through which natural selection could fix an initially plastic trait during GA. These mechanisms could also explain how GA may contribute to cryptic genetic variation that can subsequently be coopted into other phenotypes or traits, but also lead to nonadaptive responses. We outline the predicted patterns of genetic and transcriptional divergence accompanying flexible stem radiations. The analysis of such patterns of (retained) adaptive and nonadaptive plastic responses within and across radiating lineages can inform on the state of ongoing GA. We conclude that, depending on the stability of the environment, the molecular architecture underlying plastic traits can facilitate diversification, followed by fixation and consolidation of an adaptive phenotype and degeneration of nonadaptive ones. Additionally, the process of GA may increase the cryptic genetic variation of populations, which on one hand may serve as substrate for evolution, but on another may be responsible for nonadaptive responses that consolidate local allopatry and thus reproductive isolation.

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Section: Phenotypic Plasticity's Effect On Evolution and Speciationmentioning

confidence: 99%

Section: Phenotypic Plasticity's Effect On Evolution and Speciationmentioning

confidence: 99%

How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

2016

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“…Recent advances in next-generation sequencing technologies and the successful utilization of RNA interference (RNAi) have enabled researchers to delve into the genetic mechanisms underlying the growth, expression, and condition-dependence of these traits. Several recent studies focusing on horns in scarab beetles have revealed many of the genetic mechanisms regulating horn development, growth, and condition-dependence [ 15 – 17 ]. Because of their sex-specific expression, the sex determination genes of insects, which are highly conserved across the arthropods and animals in general [ 18 ], are particularly important to understanding the development of sexually selected weapon traits [ 17 ].…”

Section: Introductionmentioning

confidence: 99%

Identification and functional analyses of sex determination genes in the sexually dimorphic stag beetle Cyclommatus metallifer

et al. 2016

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BackgroundGenes in the sex determination pathway are important regulators of sexually dimorphic animal traits, including the elaborate and exaggerated male ornaments and weapons of sexual selection. In this study, we identified and functionally analyzed members of the sex determination gene family in the golden metallic stag beetle Cyclommatus metallifer, which exhibits extreme differences in mandible size between males and females.ResultsWe constructed a C. metallifer transcriptomic database from larval and prepupal developmental stages and tissues of both males and females. Using Roche 454 pyrosequencing, we generated a de novo assembled database from a total of 1,223,516 raw reads, which resulted in 14,565 isotigs (putative transcript isoforms) contained in 10,794 isogroups (putative identified genes). We queried this database for C. metallifer conserved sex determination genes and identified 14 candidate sex determination pathway genes. We then characterized the roles of several of these genes in development of extreme sexual dimorphic traits in this species. We performed molecular expression analyses with RT-PCR and functional analyses using RNAi on three C. metallifer candidate genes – Sex-lethal (CmSxl), transformer-2 (Cmtra2), and intersex (Cmix). No differences in expression pattern were found between the sexes for any of these three genes. In the RNAi gene-knockdown experiments, we found that only the Cmix had any effect on sexually dimorphic morphology, and these mimicked the effects of Cmdsx knockdown in females. Knockdown of CmSxl had no measurable effects on stag beetle phenotype, while knockdown of Cmtra2 resulted in complete lethality at the prepupal period. These results indicate that the roles of CmSxl and Cmtra2 in the sex determination cascade are likely to have diverged in stag beetles when compared to Drosophila. Our results also suggest that Cmix has a conserved role in this pathway. In addition to those three genes, we also performed a more complete functional analysis of the C. metallifer dsx gene (Cmdsx) to identify the isoforms that regulate dimorphism more fully using exon-specific RNAi. We identified a total of 16 alternative splice variants of the Cmdsx gene that code for up to 14 separate exons. Despite the variation in RNA splice products of the Cmdsx gene, only four protein isoforms are predicted. The results of our exon-specific RNAi indicated that the essential CmDsx isoform for postembryonic male differentiation is CmDsxB, whereas postembryonic female specific differentiation is mainly regulated by CmDsxD.ConclusionsTaken together, our results highlight the importance of studying the function of highly conserved sex determination pathways in numerous insect species, especially those with dramatic and exaggerated sexual dimorphism, because conservation in protein structure does not always translate into conservation in downstream function.Electronic supplementary materialThe online version of this article (doi:10.1186/s12864-016-2522-8) contains supplementary material, which is ...

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“…In weaponed beetles, the function of dsx has been examined in four species: Onthophagus taurus and O. sagitarius (Scarabaeoidea, Scarabaeidae 5 ), Trypoxylus dichotomus (Scarabaeoidea, Scarabaeidae 6 ), and Cyclommatus metallifer (Scarabaeoidea, Lucanidae 7 ). Although it is unlikely that the weapons of these beetles share a common evolutionary origin 11 , all have their sex-specific expression organized by Dsx (reviewed in 3 12 ). However, all of these beetles are also closely related, belonging to the superfamily Scarabaeoidea, and functional studies of dsx in weapon trait expression outside of the Scarabaeoidea have been limited.…”

Section: Sexually Dimorphic Weapons In Beetlesmentioning

confidence: 99%

Molecular cloning and functional characterization of the sex-determination gene doublesex in the sexually dimorphic broad-horned beetle Gnatocerus cornutus (Coleoptera, Tenebrionidae)

Gotoh

Ishiguro

Nishikawa

et al. 2016

Sci Rep

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Various types of weapon traits found in insect order Coleoptera are known as outstanding examples of sexually selected exaggerated characters. It is known that the sex determination gene doublesex (dsx) plays a significant role in sex-specific expression of weapon traits in various beetles belonging to the superfamily Scarabaeoidea. Although sex-specific weapon traits have evolved independently in various Coleopteran groups, developmental mechanisms of sex-specific expression have not been studied outside of the Scarabaeoidea. In order to test the hypothesis that dsx-dependent sex-specific expression of weapon traits is a general mechanism among the Coleoptera, we have characterized the dsx in the sexually dimorphic broad-horned beetle Gnatocerus cornutus (Tenebrionidea, Tenebirionidae). By using molecular cloning, we identified five splicing variants of Gnatocerus cornutus dsx (Gcdsx), which are predicted to code four different isoforms. We found one male-specific variant (GcDsx-M), two female-specific variants (GcDsx-FL and GcDsx-FS) and two non-sex-specific variants (correspond to a single isoform, GcDsx-C). Knockdown of all Dsx isoforms resulted in intersex phenotype both in male and female. Also, knockdown of all female-specific isoforms transformed females to intersex phenotype, while did not affect male phenotype. Our results clearly illustrate the important function of Gcdsx in determining sex-specific trait expression in both sexes.

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Development and evolution of insect polyphenisms: novel insights through the study of sex determination mechanisms

Cited by 11 publications

References 33 publications

How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

How plasticity, genetic assimilation and cryptic genetic variation may contribute to adaptive radiations

Identification and functional analyses of sex determination genes in the sexually dimorphic stag beetle Cyclommatus metallifer

Molecular cloning and functional characterization of the sex-determination gene doublesex in the sexually dimorphic broad-horned beetle Gnatocerus cornutus (Coleoptera, Tenebrionidae)

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