Insulin Signaling Mediates Sexual Attractiveness in Drosophila

Kuo, Tsung Han; Fedina, Tatyana Y.; Hansen, Ingrid Myrnes; Dreisewerd, Klaus; Dierick, Herman A.; Yew, Joanne Y.; Pletcher, Scott D.

doi:10.1371/journal.pgen.1002684

Cited by 80 publications

(110 citation statements)

References 54 publications

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“…By contrast, we show here that such links can emerge from a model of adaptive signalling, and only when signalling is differentially costly for low-quality individuals. This suggests that, contrary to recent claims [21,22,29,30], evidence for a strong causal link between individual quality and signal size does not diminish the role of costs in the maintenance of honesty. Our results imply that index signals fit neatly into the framework of costly signalling theory (see also [31]).…”

Section: (A) Index Signals Costly Signalling Theory and The Handicapcontrasting

confidence: 91%

The evolution of index signals to avoid the cost of dishonesty

2014

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Animals often convey useful information, despite a conflict of interest between the signaller and receiver. There are two major explanations for such 'honest' signalling, particularly when the size or intensity of signals reliably indicates the underlying quality of the signaller. Costly signalling theory (including the handicap principle) predicts that dishonest signals are too costly to fake, whereas the index hypothesis predicts that dishonest signals cannot be faked. Recent evidence of a highly conserved causal link between individual quality and signal growth appears to bolster the index hypothesis. However, it is not clear that this also diminishes costly signalling theory, as is often suggested. Here, by incorporating a mechanism of signal growth into costly signalling theory, we show that index signals can actually be favoured owing to the cost of dishonesty. We conclude that costly signalling theory provides the ultimate, adaptive rationale for honest signalling, whereas the index hypothesis describes one proximate (and potentially very general) mechanism for achieving honesty.

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Section: (A) Index Signals Costly Signalling Theory and The Handicapcontrasting

confidence: 91%

The evolution of index signals to avoid the cost of dishonesty

2014

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“…Regarding the feedback regulation of GSCs, we note that the systemic downregulation of IIS dramatically extends the reproductive span (Luo et al, 2010); however, this is accompanied by a range of life-extending somatic side-effects that conversely impair sexual attractiveness, such as reduced motility, an abnormal appearance and aberrant pheromone secretion (Gems et al, 1998;Kuo et al, 2012). One appealing possibility is that germline-restricted IIS output control may have evolved to specifically delay reproductive ageing, or at least preserve germline integrity by slowing stem cell divisions, without otherwise compromising attractiveness.…”

Section: Germline-specific Iis Counteractionmentioning

confidence: 98%

daf-18/PTEN locally antagonizes insulin signalling to couple germline stem cell proliferation to oocyte needs inC. elegans

2015

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During development, stem cell populations rapidly proliferate to populate the expanding tissues and organs. During this phase, nutrient status, by systemically affecting insulin/IGF-1 signalling, largely dictates stem cell proliferation rates. In adults, however, differentiated stem cell progeny requirements are generally reduced and vary according to the spatiotemporal needs of each tissue. We demonstrate here that differential regulation of germline stem cell proliferation rates in Caenorhabditis elegans adults is accomplished through localized neutralization of insulin/IGF-1 signalling, requiring DAF-18/PTEN, but not DAF-16/FOXO. Indeed, the specific accumulation of oocytes, the terminally differentiated stem cell progeny, triggers a feedback signal that locally antagonizes insulin/ IGF-1 signalling outputs in the germ line, regardless of their systemic levels, to block germline stem cell proliferation. Thus, during adulthood, stem cells can differentially respond within tissues to otherwise equal insulin/IGF-1 signalling inputs, according to the needs for production of their immediate terminally differentiated progeny.

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“…Drosophila insulin-like peptides (DILPs) are necessary for vitellogenesis (Richard et al 2005). DILPs regulate stem-cell division in the ovary (LaFever and Drummond-Barbosa 2005) and mediate sexual attractiveness (Kuo et al 2012). Another neuropeptide expressed in the pars intercerebralis is SIFamide that modulates courtship (Terhzaz et al 2007).…”

Section: Implications Of Neprilysins 1-5 Expression Patternsmentioning

confidence: 99%

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

et al. 2014

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Members of the M13 class of metalloproteases have been implicated in diseases and in reproductive fitness. Nevertheless, their physiological role remains poorly understood. To obtain a tractable model with which to analyze this protein family's function, we characterized the gene family in Drosophila melanogaster and focused on reproductive phenotypes. The D. melanogaster genome contains 24 M13 class protease homologs, some of which are orthologs of human proteases, including neprilysin. Many are expressed in the reproductive tracts of either sex. Using RNAi we individually targeted the five Nep genes most closely related to vertebrate neprilysin, Nep1-5, to investigate their roles in reproduction. A reduction in Nep1, Nep2, or Nep4 expression in females reduced egg laying. Nep1 and Nep2 are required in the CNS and the spermathecae for wild-type fecundity. Females that are null for Nep2 also show defects as hosts of sperm competition as well as an increased rate of depletion for stored sperm. Furthermore, eggs laid by Nep2 mutant females are fertilized normally, but arrest early in embryonic development. In the male, only Nep1 was required to induce normal patterns of female egg laying. Reduction in the expression of Nep2-5 in the male did not cause any dramatic effects on reproductive fitness, which suggests that these genes are either nonessential for male fertility or perform redundant functions. Our results suggest that, consistent with the functions of neprilysins in mammals, these proteins are also required for reproduction in Drosophila, opening up this model system for further functional analysis of this protein class and their substrates. P ROTEASES play key roles in diverse physiological systems. One such family of metalloproteases, the M13 class of neutral endopeptidases, consists mainly of membranebound zinc proteases that are involved in the processing of neuropeptides and peptide hormones (reviewed in Turner et al. 2000;Turner et al. 2001;Bland et al. 2008). In mammals, seven members of this family have been identified, of which neprilysin (NEP) and endothelin converting enzyme (ECE) are the best studied. These proteins have been implicated in various diseases including cardiovascular disease (Segura and Ruilope 2011;Wick et al. 2011), Alzheimer's disease (Mulder et al. 2012;Klein et al. 2013), inflammation and inflammatory disorders (Wong et al. 2011), and cancer (Smollich et al. 2007;Maguer-Satta et al. 2011).In addition to their role in disease, NEPs are essential for development and reproduction in mammals. The mammalian Neprilysin-2, called NL1 in mice, is highly expressed in the testis. NL1-deficient males sire fewer pups, even though spermatogenesis appears to be unaffected (Carpentier et al. 2004). In females, NEP expression in the uterus is modulated by estrogen treatment in rats (Pinto et al. 1999) and during the estrogen/progesterone cycle in humans (Head et al. 1993). In female rats and mice, controlled degradation of tachykinins, particularly substance-P, by NEP in the uterus ...

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Insulin Signaling Mediates Sexual Attractiveness in Drosophila

Cited by 80 publications

References 54 publications

The evolution of index signals to avoid the cost of dishonesty

The evolution of index signals to avoid the cost of dishonesty

daf-18/PTEN locally antagonizes insulin signalling to couple germline stem cell proliferation to oocyte needs inC. elegans

Neprilysins: An Evolutionarily Conserved Family of Metalloproteases That Play Important Roles in Reproduction in Drosophila

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