Indirect genetic effects and sexual conflicts: partner genotype influences multiple morphological and behavioural reproductive traits in a flatworm

The expression of an individual's phenotypic traits can be influenced by genes expressed in its social partners. Theoretical models predict that such indirect genetic effects (IGEs) on reproductive traits should play an important role in determining the evolutionary outcome of sexual conflict. However, empirical tests of (i) whether reproductive IGEs exist, (ii) how they vary among genotypes, and (iii) whether they are uniform for different types of reproductive traits are largely lacking. We addressed this in a series of experiments in the simultaneously hermaphroditic flatworm Macrostomum lignano. We found strong evidence for IGEs on both morphological and behavioral reproductive traits. Partner genotype had a significant impact on the testis size of focal individuals—varying up to 2.4-fold—suggesting that IGEs could mediate sexual conflicts that target the male sex function. We also found that time to first copulation was affected by a genotype × genotype interaction between mating partners, and that partner genotype affected the propensity to copulate and perform the postcopulatory suck behavior, which may mediate conflicts over the fate of received ejaculate components. These findings provide clear empirical evidence for IGEs on multiple behavioral and morphological reproductive traits, which suggests that the evolutionary dynamics of these traits could be altered by genes contained in the social environment.PostprintPeer reviewe

Causes and Consequences of External Female Genital Mutilation

Sexual selection favours traits that confer a competitive advantage in access to mates and to their gametes. This results in males evolving a wide array of adaptations that may be conflictual with female’s interests and even to collateral negative effects on female’s lifespan or reproductive success. Harmful male adaptations are diverse and can be extreme. For example, males of various species evolved adaptations that incur physical damage to the female during copulation, referred to as traumatic mating. Most of these adaptations provide males with a competitive fertilization advantage due to the injection of sperm or non-sperm compounds through the wound. In the spider taxonomical literature, alterations of external genital structures have been reported in females and may result from male inflicted damage during copulation. Contrarily to other cases of traumatic mating, the transfer of sperm or non-sperm compounds does not seem to be the target of selection for external female genital mutilation (EFGM) to evolve. Therefore, investigating EFGM may provide valuable information to extend our understanding of the evolution of harmful male adaptations. In this thesis, I explore this newly discovered phenomenon and combine empirical and theoretical approaches to investigate the causes and consequences of EFGM evolution from male and female perspectives. My findings suggest that EFGM is a natural phenomenon and is potentially widespread throughout spider taxa. I demonstrate the proximal mechanism by which the male copulatory organ mutilates the external female genitalia during genital coupling and show that the mutilation results in full monopolization of the female as mutilated females are unable to remate. Using a theoretical approach, I investigated the conditions for the evolution of EFGM. The model developed suggests that EFGM evolution is favoured for last male sperm precedence and for costs to females that can be relatively high as the male-male competition increases. I present the results of physiological measurements that suggest there is no physiological cost of genital mutilation resulting from healing and immune responses for the female. Finally, I report the results of a behavioural experiment that suggest that females have control over the mutilation and selectively allow or avoid mutilation. These findings suggest that EFGM benefits males by securing paternity, that males and females may have evolved to reduce the costs incurred by the female and that female choice may also play a role in EFGM evolution.Die sexuelle Selektion bevorzugt Merkmale, die mit einem Wettbewerbsvorteil beim Zugang zu Partnern und ihren Gameten einhergehen. Dies führt dazu, dass Männchen ein breites Spektrum an Anpassungen entwickeln, die mit den Interessen der Weibchen in Konflikt geraten und sogar negative Auswirkungen auf die Lebensdauer oder den Fortpflanzungserfolg von Weibchen haben können. Schädliche männliche Anpassungen sind mehrfach evoluiert. Zum Beispiel fügen Männchen verschiedener Arten dem Weibchen während der Kopulation körperlichen Schaden zu, was als „traumatische Paarung“ bezeichnet wird. In solchen Fällen wurde gezeigt, dass die Männchen einen Vorteil in der Spermienkonkurrenz durch die Injektion von Spermien oder akzessorischen, manipulativen Substanzen durch die Wunde erzielen. Die taxonomische Spinnenliteratur enthält Berichte über veränderte äußere Genitalstrukturen von Weibchen. Diese Schäden könnten mit der Kopulation zusammenhängen und eine Strategie der Vaterschaftssicherung darstellen. Im Gegensatz zu anderen Fällen von traumatischer Paarung scheint der Transfer von Spermien oder Nichtspermienverbindungen die Evolution der externen weiblichen Genitalverstümmelung (external female genital mutilation „EFGM“) nicht vorangetrieben zu haben. Daher kann die Untersuchung von EFGM wertvolle Informationen liefern, um unser Verständnis der Evolution schädlicher männlicher Anpassungen zu erweitern. In dieser Arbeit untersuche ich das neu entdeckte Phänomen von EFGM und kombiniere empirische und theoretische Ansätze, um die Ursachen und Folgen der EFGM-Evolution aus männlicher und weiblicher Perspektiven zu erhellen. Meine Ergebnisse zeigen, dass EFGM ein natürlich vorkommendes Phänomen ist und vielen Spinnen-Taxa verbreitet ist. Ich kläre den proximalen Mechanismus, durch den das männliche Kopulationsorgan die äußeren weiblichen Genitalien während der Genitalkopplung verändert, mit Hilfe von Micro-Ct und Verhaltensversuchen auf. Die Entfernung einer für die Verhakung der Genitalien notwendigen Struktur führt zu einer vollständigen Monopolisierung des Weibchens. Verstümmelte Weibchen sind nicht in der Lage, sich erneut zu verpaaren. Mit einem theoretischen Ansatz untersuchte ich die Bedingungen für die Evolution von EFGM. Das Modell legt nahe, dass EFGM bei Arten mit Letzter-Männchen-Spermienpriorität schnell evoluieren kann – auch dann, wenn die Kosten für Weibchen hoch sind. Ich präsentiere weiterhin die Ergebnisse physiologischer Messungen, bei denen keine signifikanten physiologischen Kosten für Genitalverstümmelungen gefunden wurden. Die Ergebnisse eines Verhaltensexperiments zeigen weiterhin, dass Weibchen die Wahrscheinlichkeit des Auftretens der Verstümmelung kontrollieren können. Diese Ergebnisse sprechen dafür, dass EFGM selektive Vorteile bei der Vaterschaftssicherung mit sich bringt, dass es Koevolution zwischen Männche und Weibchen gibt, die zu reduzierten Kosten für Weibchen führte, und dass die Wahl der Partner durch die Weibchen das Auftreten von EFGM bestimmen kann

Mouginot_Uhl_Data_072019

Data produced in a lab experiment with individual spiders collected in the field

Evolution of external female genital mutilation : why do males harm their mates?

Sperm competition may select for male reproductive traits that influence female mating or oviposition rate. These traits may induce fitness costs to the female; however, they may be costly for the males as well as any decrease in female fitness also affects male fitness. Male adaptations to sperm competition manipulate females by altering not only female behaviour or physiology, but also female morphology. In orb-weaving spiders, mating may entail mutilation of external structures of the female genitalia, which prevents genital coupling with subsequent males. Here, we present a game theoretical model showing that external female genital mutilation is favoured even under relatively high costs of mutilation, and that it is favoured by a high number of mate encounters per female and last-male sperm precedence.peerReviewe

Non‐reproducible signals of adaptation to elevation between open and understorey microhabitats in snapdragon plants

International audienceExperimental studies on local adaptation rarely investigate how different environmental variables might modify signals of adaptation or maladaptation. In plant common garden experiments, signals of adaptation or maladaptation to elevation are usually investigated in open habitats under full light. However, most plants inhabit heterogeneous habitats where environmental conditions differ. Understorey microhabitats are common and differ in terms of tree shade, temperature, water availability, microbiota, allelochemicals etc. Germination is a fitness-related trait of major importance for the adaptation of plants to contrasted climate conditions. It is affected by shade in snapdragon plants (Antirrhinum majus) and many other plant species. Here, we tested for the reproducibility of signals extrapolated from germination results between open and understorey microhabitats in two parapatric snapdragon plant subspecies (A. m. striatum and A. m. pseudomajus) characterized by a similar elevation range by using common garden experiments at different elevations. Signals observed under one microhabitat systematically differed in the other. Most scenarios could be inferred, with signals either shifting, appearing or disappearing between different environments. Our findings imply that caution should be taken when extrapolating the evolutionary significance of these types of experimental signals because they are not stable from one local environmental condition to the next. Forecasting the ability of plants to adapt to environmental changes based on common garden and reciprocal transplant experiments must account for the multivariate nature of the environment

Wild snapdragon plant pedigree sheds light on limited connectivity enhanced by higher migrant reproductive success in a fragmented landscape

Background: In contrast with historical knowledge, a recent view posits that a non-negligible proportion of populations thrive in a fragmented landscape. One underlying mechanism is the maintenance of functional connectivity, i.e., the net flow of individuals or their genes moving among suitable habitat patches. Alternatively, functional connectivity might be typically limited but enhanced by a higher reproductive success of migrants. Methods: We tested for this hypothesis in wild snapdragon plants inhabiting six patches separated by seawater in a fragmented Mediterranean scrubland landscape. We reconstructed their pedigree by using a parentage assignment method based on microsatellite genetic markers. We then estimated functional connectivity and the reproductive success of plants resulting from between-patch dispersal events. Results: We found that wild snapdragon plants thrived in this fragmented landscape, although functional connectivity between habitat patches was low (i.e. 2.9%). The progeny resulting from between-patch dispersal events had a higher reproductive success than residents. Conclusion: Our findings imply that low functional connectivity in a fragmented landscapes may have been enhanced by higher reproductive success after migration. This original mechanisms might be partly compensating the negative impact of fragmentation

Wild snapdragon plant pedigree sheds light on limited connectivity enhanced by higher migrant reproductive success in a fragmented landscape

Background: In contrast with historical knowledge, a recent view posits that a non-negligible proportion of populations might respond positively to habitat fragmentation. Populations might thrive in a fragmented landscape if functional connectivity, i.e., the net flow of individuals or their genes moving among suitable habitat patches, is not restricted. Alternatively, functional connectivity might be typically limited but enhanced by a higher reproductive success of migrants. Methods: We tested for this hypothesis in wild snapdragon plants inhabiting six patches separated by seawater in a fragmented Mediterranean scrubland landscape. We reconstructed their pedigree by using a parentage assignment method based on microsatellite genetic markers. We then estimated functional connectivity and the reproductive success of plants resulting from between-patch dispersal events. Results: We found that wild snapdragon plants thrived in this fragmented landscape, although functional connectivity between habitat patches was weak (i.e. 2.9%). The progeny resulting from between-patch dispersal events had a higher reproductive success than residents. Conclusion: Our findings expose a remarkable aspect of fragmented landscapes, where weak functional connectivity was enhanced by higher reproductive success after migration. This process might have the potential to compensate at least partly the negative impact of fragmentation

Indirect genetic effects and sexual conflicts: partner genotype influences multiple morphological and behavioural reproductive traits in a flatworm

The expression of an individual's phenotypic traits can be influenced by genes expressed in its social partners. Theoretical models predict that such indirect genetic effects (IGEs) on reproductive traits should play an important role in determining the evolutionary outcome of sexual conflict. However, empirical tests of (i) whether reproductive IGEs exist, (ii) how they vary among genotypes, and (iii) whether they are uniform for different types of reproductive traits are largely lacking. We addressed this in a series of experiments in the simultaneously hermaphroditic flatworm Macrostomum lignano. We found strong evidence for IGEs on both morphological and behavioral reproductive traits. Partner genotype had a significant impact on the testis size of focal individuals—varying up to 2.4-fold—suggesting that IGEs could mediate sexual conflicts that target the male sex function. We also found that time to first copulation was affected by a genotype × genotype interaction between mating partners, and that partner genotype affected the propensity to copulate and perform the postcopulatory suck behavior, which may mediate conflicts over the fate of received ejaculate components. These findings provide clear empirical evidence for IGEs on multiple behavioral and morphological reproductive traits, which suggests that the evolutionary dynamics of these traits could be altered by genes contained in the social environment

Phenotypic Response to Light Versus Shade Associated with DNA Methylation Changes in Snapdragon Plants (Antirrhinum majus)

The phenotypic plasticity of plants in response to change in their light environment, and in particularly, to shade is a schoolbook example of ecologically relevant phenotypic plasticity with evolutionary adaptive implications. Epigenetic variation is known to potentially underlie plant phenotypic plasticity. Yet, little is known about its role in ecologically and evolutionary relevant mechanisms shaping the diversity of plant populations in nature. Here we used a reference-free reduced representation bisulfite sequencing method for non-model organisms (epiGBS) to investigate changes in DNA methylation patterns across the genome in snapdragon plants (Antirrhinum majus L.). We exposed plants to sunlight versus artificially induced shade in four highly inbred lines to exclude genetic confounding effects. Our results showed that phenotypic plasticity in response to light versus shade shaped vegetative traits. They also showed that DNA methylation patterns were modified under light versus shade, with a trend towards global effects over the genome but with large effects found on a restricted portion. We also detected the existence of a correlation between phenotypic and epigenetic variation that neither supported nor rejected its potential role in plasticity. While our findings imply epigenetic changes in response to light versus shade environments in snapdragon plants, whether these changes are directly involved in the phenotypic plastic response of plants remains to be investigated. Our approach contributed to this new finding but illustrates the limits in terms of sample size and statistical power of population epigenetic approaches in non-model organisms. Pushing this boundary will be necessary before the relationship between environmentally induced epigenetic changes and phenotypic plasticity is clarified for ecologically relevant mechanisms with evolutionary implications

No evidence of direct contribution of adult plant stages to climate adaptation in snapdragon plants

International audienceSignatures of local adaptation have been found at all life stages in plants. Yet, the contribution of later plant stages is rarely disentangled from the influence of early-life stages. Here, we investigate the direct contribution of adult plant stages to climate adaptation in two subspecies of snapdragon plants (Antirrhinum majus), while growth conditions have been homogenized at early-life stages. We compared genetic variation in fitness proxies (i.e. flowering, number of flowers and survival) and phenotypic traits in adult plants of eight populations of A. m. pseudomajus and seven populations of A. m. striatum, in two common garden experiments at high and low elevations. We found no evidence of adaptation to elevation in adult plants in both subspecies. Populations of low-elevation habitats outperformed populations of high-elevation habitats in all gardens. The effects of phenotypic traits on fitness components were similar at high and low elevation, suggesting no divergent selection along elevation. Different traits had an effect on fitness proxies in A. m. striatum and A. m. pseudomajus, suggesting that different mechanisms are at play in these two subspecies. Our findings suggest that there is no direct contribution of adult plant stages to climate adaptation in snapdragon plants and that adaptive processes potentially differ at the scale of A. majus subspecies