Seminal Fluid-Mediated Manipulation of Post-mating Behavior in a Simultaneous Hermaphrodite

Patlar, Bahar; Weber, Michael; Temizyürek, Tim; Ramm, Steven A.

doi:10.1016/j.cub.2019.11.018

Cited by 30 publications

(51 citation statements)

References 82 publications

(143 reference statements)

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“…They are kept under standard conditions on a 14:10 light:dark cycle at 60% relative humidity and a constant temperature of 20°C. All the animals used in this experiment as knockdown/control donors and as recipients (see below) belonged to the highly inbred DV1 line (Janicke et al 2013) that was previously used to identify and functionally characterize putative seminal fluid candidates (Weber et al 2018; Weber et al, submitted; Patlar et al, submitted).…”

Section: Methodsmentioning

confidence: 99%

“…Because the same two candidate transcripts, Mlig-pro46 and Mlig-pro63, were also positively loaded on an additional axis of seminal fluid variation, PC3, and this was positively correlated with suck propensity in the pairs environment (Patlar et al, submitted), we further investigated whether RNAi knockdown also impacted on partner suck behavior.…”

Section: Methodsmentioning

confidence: 99%

“…However, given that this screen identified only a minority of candidate SFPs modulating fertility or sperm competitiveness, and that all of these effects have not yet been verified after controlling for multiple testing, this suggests that more targeted methods may be beneficial to first prioritise candidates mediating specific effects. Patlar et al (submitted) adopted precisely such an approach, using quantitative genetics to identify six candidate SFPs likely to affect the post-mating ‘suck’ behavior of sperm recipients, based on a negative genetic correlation between SFP transcript expression (Patlar et al 2018) and suck propensity. The suck behavior in M. lignano is a striking response to ejaculate recipient, in which the worm places its pharynx over its female genital opening and appears to attempt to suck out its contents, suggesting this trait has evolved in the context of sexual conflict over control of the received ejaculate (Schärer et al 2004a; Vizoso et al 2010; Scharer et al 2011; Marie-Orleach et al 2013).…”

Section: Introductionmentioning

confidence: 99%

“…The suck behavior in M. lignano is a striking response to ejaculate recipient, in which the worm places its pharynx over its female genital opening and appears to attempt to suck out its contents, suggesting this trait has evolved in the context of sexual conflict over control of the received ejaculate (Schärer et al 2004a; Vizoso et al 2010; Scharer et al 2011; Marie-Orleach et al 2013). RNAi-induced knockdown of two of the six SFP candidate genes, Mlig-pro31 and Mlig-pro32, caused a substantially increased suck propensity of mating partners, suggesting that these proteins indeed manipulate mating partners and may thereby mediate sexual conflict over ejaculate fate, but no clear effect on paternity outcomes in a standardized defensive sperm competition assay (Patlar et al, submitted).…”

Section: Introductionmentioning

confidence: 99%

“…The quantitative genetic approach adopted by Patlar et al (submitted) provides a powerful framework to identify candidates for subsequent screening of SFP-mediated effects in a targeted manner. We therefore here adopted this same method, enabling us to identify two candidate SFPs, Mlig-pro46 and Mlig-pro63, potentially affecting two behavioural phenotypes of interest: partner re-mating behavior and the propensity for partners to exhibit the suck behavior (see Methods).…”

Section: Introductionmentioning

confidence: 99%

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Effects of two seminal fluid proteins on post-mating behavior in the simultaneously hermaphroditic flatwormMacrostomum lignano

Weber

Patlar

Ramm

2019

Preprint

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Along with sperm, in many taxa male ejaculates also contain a complex mixture of proteins, peptides and other substances found in seminal fluid. Once seminal fluid proteins (SFPs) are transferred to the mating partner, they play crucial roles in mediating post-mating sexual selection, since they can modulate the partner’s behavior and physiology in ways that influence the reproductive success of both partners. One way in which sperm donors can maximize their own reproductive success is by changing the partners’ (sperm recipient’s) postcopulatory behavior to prevent or delay re-mating, thereby decreasing the likelihood or intensity of sperm competition. We therefore adopted a quantitative genetic approach combining gene expression and behavioral data to identify candidates that could mediate such a response in the simultaneously hermaphroditic flatwormMacrostomum lignano. We identified two putative SFPs - Mlig-pro46 and Mlig-pro63 - that exhibit a negative genetic correlation between transcript expression and mating frequency. Importantly, however, in one of the two different group sizes, differing in their sperm competition level, in which we measured genetic correlations, these same two transcripts are also linked to a second post-mating behavior inM. lignano, namely the ‘suck’ behavior of recipients in which, upon ejaculate receipt, the worm places its pharynx over its female genital opening and appears to attempt to remove ejaculate components. To therefore investigate directly whether these two candidates manipulate partner behavior, and test whether this impacts on competitive fertilization success, we performed a manipulative experiment using RNA interference-induced knockdown to ask how loss of Mlig-pro46 and Mlig-pro63 expression, singly and in combination, affects mating frequency, partner suck propensity and both defensive and offensive sperm competitive ability (P1andP2, respectively). None of the knock-down treatments impacted strongly on mating frequency or sperm competitive ability, but the knock-down of Mlig-pro63 resulted in a significantly decreased ‘suck’ propensity of mating partners. This suggests that Mlig-pro63 may normally act as a cue in the ejaculate to trigger recipient suck behavior, though the functional and adaptive significance of these two seminal proteins from a donor perspective remains enigmatic.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Effects of two seminal fluid proteins on post-mating behavior in the simultaneously hermaphroditic flatwormMacrostomum lignano

Weber

Patlar

Ramm

2019

Preprint

Self Cite

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The repeatable opportunity for selection differs between pre- and postcopulatory fitness components

2021

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In species with multiple mating, intense sexual selection may occur both before and after copulation. However, comparing the strength of pre- and postcopulatory selection is challenging, because (i) postcopulatory processes are generally difficult to observe and (ii) the often-used opportunity for selection (I) metric contains both deterministic and stochastic components. Here, we quantified pre- and postcopulatory male fitness components of the simultaneously hermaphroditic flatworm, Macrostomum lignano. We did this by tracking fluorescent sperm—using transgenics—through the transparent body of sperm recipients, enabling to observe postcopulatory processes in vivo. Moreover, we sequentially exposed focal worms to three independent mating groups, and in each assessed their mating success, sperm-transfer efficiency, sperm fertilizing efficiency, and partner fecundity. Based on these multiple measures, we could, for each fitness component, combine the variance (I) with the repeatability (R) in individual success to assess the amount of repeatable variance in individual success—a measure we call the repeatable opportunity for selection (IR). We found higher repeatable opportunity for selection in sperm-transfer efficiency and sperm fertilizing efficiency compared to mating success, which clearly suggests that postcopulatory selection is stronger than precopulatory selection. Our study demonstrates that the opportunity for selection contains a repeatable deterministic component, which can be assessed and disentangled from the often large stochastic component, to provide a better estimate of the strength of selection.

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Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

2022

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Traumatic insemination is a mating behavior during which the (sperm) donor uses a traumatic intromittent organ to inject an ejaculate through the epidermis of the (sperm) recipient, thereby frequently circumventing the female genitalia. Traumatic insemination occurs widely across animals, but the frequency of its evolution, the intermediate stages via which it originates, and the morphological changes that such shifts involve remain poorly understood. Based on observations in 145 species of the free-living flatworm genus Macrostomum, we identify at least nine independent evolutionary origins of traumatic insemination from reciprocal copulation, but no clear indication of reversals. These origins involve convergent shifts in multivariate morphospace of male and female reproductive traits, suggesting that traumatic insemination has a canalizing effect on morphology. We also observed sperm in both the sperm receiving organ and within the body tissue of two species. These species had intermediate trait values indicating that traumatic insemination evolves through initial internal wounding during copulation. Finally, signatures of malefemale coevolution of genitalia across the genus indicate that sexual selection and sexual conflict drive the evolution of traumatic insemination, because it allows donors to bypass postcopulatory control mechanisms of recipients.

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Seminal Fluid-Mediated Manipulation of Post-mating Behavior in a Simultaneous Hermaphrodite

Cited by 30 publications

References 82 publications

Effects of two seminal fluid proteins on post-mating behavior in the simultaneously hermaphroditic flatwormMacrostomum lignano

Effects of two seminal fluid proteins on post-mating behavior in the simultaneously hermaphroditic flatwormMacrostomum lignano

The repeatable opportunity for selection differs between pre- and postcopulatory fitness components

Frequent origins of traumatic insemination involve convergent shifts in sperm and genital morphology

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