Evolution of the neural sex‐determination system in insects: does <i>fruitless</i> homologue regulate neural sexual dimorphism in basal insects?

Watanabe, Takayuki

doi:10.1111/imb.12590

Cited by 16 publications

(5 citation statements)

References 83 publications

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“…The putative sequences of Pmfru-1 and Pmfru-2 exhibited highly conserved BTB domain and ZF domains. Fruitless have been identified in several insect and crustacean species, including many species in Drosophilidae, Nasonia vitripennis , Gryllus bimaculatus , and Chinese mitten crab E. sinensis ( Bertossa, Van de Zande & Beukeboom, 2009 ; Li et al, 2017 ; Ryner et al, 1996 ; Watanabe, 2019 ; Zollman et al, 1994 ). We showed that Pmfru-1 and Pmfru-2 could be derived from the same genomic locus by mutually-exclusive-exons alternative splicing of the Pmfru pre-mRNA ( Fig.…”

Section: Discussionmentioning

confidence: 99%

Molecular characterization and expression profiling of transformer 2 and fruitless-like homologs in the black tiger shrimp, Penaeus monodon

Thaijongrak

Chotwiwatthanakun

Laphyai

et al. 2022

PeerJ

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Transformer 2 (tra 2) and fruitless (fru) genes have been proven to play a key role in sex determination pathways in many Arthropods, including insects and crustaceans. In this study, a paralog of P. monodon tra 2 (Pmtra 2), P. monodon ovarian associated transformer 2 (PmOvtra 2) and 2 isoforms of P. monodon fruitless-like gene (Pmfru-1 and Pmfru-2) were identified and characterized. The full cDNA sequence of PmOvtra 2 consisted of 1,774 bp with the longest open reading frame (ORF) of 744 bp encoding for 247 amino acids. The PmOvtra 2 exhibited a predicted RNA-recognition motif (RRM) domain and two arginine-serine (RS) regions, suggesting its function in RNA splicing. The full cDNA sequence of Pmfru-1 consisted of 1,306 bp with 1,182 bp ORF encoding for 393 amino acids, whereas the full cDNA sequence of Pmfru-2 consisted of 1,858 bp with 1,437 bp ORF encoding 478 amino acids. The deduced amino acid sequences of Pmfru-1 and Pmfru-2 exhibited highly conserved domains of Fru proteins, including Broad-complex, Tramtrack and Bric-a-brac (BTB), and zinc finger (ZF) domains. In addition, Pmfru-1 and Pmfru-2 were suggestively originated from the same single genomic locus by genomic sequence analysis. Specifically, Pmfru pre-mRNA was alternatively spliced for Pmfru-1 and Pmfru-2 to include mutually exclusive exon 7 and exon 6, respectively. Temporal and spatial expression of PmOvtra 2, Pmfru-1, and Pmfru-2 were also investigated by qPCR. The results showed that all were expressed in early developmental stages with undifferentiated gonads starting from nauplius until postlarvae. The expression of PmOvtra 2 started at nauplius stage and gradually increased from mysis to postlarvae (PL) 1. However, the expression of Pmfru-1 was low at the nauplii stage and slightly increased from protozoea to PL5, whereas the expression of Pmfru-2 maintained a low level from nauplius to mysis and then gradually increased at the PL stages. Expressions of PmOvtra 2, Pmfru-1, and Pmfru-2 were detected in various tissues including nervous tissue, gill, heart, hepatopancreas, gut, and gonads. Interestingly, the sexually dimorphic expression of PmOvtra 2, Pmfru-1, and Pmfru-2 was demonstrated in fully developed gonads in which the ovary showed significantly higher expressions than the testis. The great difference in the expression pattern of PmOvtra 2, Pmfru-1, and Pmfru-2 in the ovary and testis suggested their roles in the female sex determination in P. monodon.

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Section: Discussionmentioning

confidence: 99%

Molecular characterization and expression profiling of transformer 2 and fruitless-like homologs in the black tiger shrimp, Penaeus monodon

Thaijongrak

Chotwiwatthanakun

Laphyai

et al. 2022

PeerJ

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“…The role of Fru in controlling brain organization for male sexual behaviour in other insects is largely unknown. Despite this, recent research suggests that in basal hemimetabolous insects, Fru is not sex‐specifically spliced and is not likely to be involved in neural sex determination (Watanabe, 2019). However, even in Drosophila , all neuronal clusters expressing Dsx are either sex‐specific or sexually dimorphic and none are sexually monomorphic (Nojima et al, 2021).…”

Section: Sex‐determination and The Birth Of Neuronsmentioning

confidence: 99%

A unique sense of smell: development and evolution of a sexually dimorphic antennal lobe – a review

Williams

Verhulst

Haverkamp

2022

Entomologia Exp Applicata

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Well-defined neural circuitries in the invertebrate nervous system have long served as model systems to address fundamental questions in neuroscience (Kandel, 2001;Masse et al., 2009). The insect antennal lobe (AL), in particular, possesses highly specialized and well-defined neural circuitries ideal for examination. In this review, we will assess how developmental processes in this brain region contribute to the evolution of sexually dimorphic pheromone circuitries within insects.Insect neurobiologists have long been fascinated by the curious anatomy of the AL, not only by its synaptic organization, but also by the functional properties of its neurons. Each AL neuron has a defined role in processing information. When combined, these neurons reconstruct the complex olfactory world of an insect (Hansson & Anton, 2000).

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“…Other studies have suggested that gynandromorphs' sexual behaviours may be more strongly influenced by the head (brain) rather than by the abdomen (reproductive organs) (Yoshizawa et al 2009). Under effect of sex-specific fruitless (fru) gene products, neurones of the insect brain form sexually dimorphic circuits, regulating sexual behaviours such as courtship and aggression (Watanabe 2019). Matsuo et al (2018) have analyzed the encephalic and antennal expression patterns of the fru gene in a Bombus ignitus gynandromorph with a bilaterally dimorphic head and thorax (left side-male, right side-female) and a uniformly masculine gaster.…”

Section: Behaviourmentioning

confidence: 99%

A bilateral gynandromorph of Discoelius dufourii (Hymenoptera, Vespidae, Zethinae): morphology and mating behaviour

Budrienė¹,

Budrys²,

Orlovskytė³

2021

JHR

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A gynandromorph is an organism combining both female- and male-type tissues. While the vast majority of studies have described the morphology of gynandromorphs, their sexual behaviours remain under-explored. We studied a predominantly bilateral gynandromorph specimen of the predatory wasp Discoelius dufourii (Hymenoptera: Vespidae: Zethinae) reared from a trap-nest. In addition to describing the morphology, we explored the gynandromorph’s response to a conspecific female, comparing it with the behavioural interactions between normal males and females of D. dufourii and the phylogenetically related D. zonalis. For most specific behavioural elements, males of both Discoelius species exhibited a greater frequency and a higher probability of occurrences of the behaviour than did females. However, aggression and plopping behaviours were prevalent in females. The gynandromorphic specimen demonstrated behavioural activities similar to those of a male, including a relatively frequent mate body antennation and an attempt to mount a female. However, it approached the female less frequently in comparison to conspecific normal males, and it did not demonstrate substrate antennation and jumping, typical of Discoelius male mating behaviour. Based on the parameters of the nest cell, the probability of the development of the gynandromorphic specimen from an unfertilized (male) egg was higher than the probability of development from a fertilized (female) egg.

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Evolution of the neural sex‐determination system in insects: does fruitless homologue regulate neural sexual dimorphism in basal insects?

Cited by 16 publications

References 83 publications

Molecular characterization and expression profiling of transformer 2 and fruitless-like homologs in the black tiger shrimp, Penaeus monodon

Molecular characterization and expression profiling of transformer 2 and fruitless-like homologs in the black tiger shrimp, Penaeus monodon

A unique sense of smell: development and evolution of a sexually dimorphic antennal lobe – a review

A bilateral gynandromorph of Discoelius dufourii (Hymenoptera, Vespidae, Zethinae): morphology and mating behaviour

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