Reproductive interference in insects

1. Reproductive interference occurs when members of different species engage in reproductive interactions, leading to a fitness cost to one or both actors. 2. These interactions can arise through signal interference (‘signal-jamming’), disrupted mate searching, heterospecific rivalry, mate choice errors, or misplaced courtship, mating attempts or copulation. 3. We present a definition of reproductive interference (RI) and discuss the extent to which a failure of species discrimination is central to a definition of RI. 4. The possible mechanisms of RI are reviewed, using a range of insect examples. 5. Some of the causes and consequences of RI are discussed, focusing in particular on mating systems and mating system evolution. 6. We conclude by considering future ways forward, highlighting the opportunities for new theory and tests of the old theory presented by reproductive interference.PostprintPeer reviewe

Safety in Numbers : How Color Morph Frequency Affects Predation Risk in an Aposematic Moth*

Polymorphic warning signals in aposematic systems are enigmatic because predator learning should favor the most common form, creating positive frequency-dependent survival. However, many populations exhibit variation in warning signals. There are various selective mechanisms that can counter positive frequency-dependent selection and lead to temporal or spatial warning signal diversification. Examining these mechanisms and their effects requires first confirming whether the most common morphs are favored at both local and regional scales. Empirical examples of this are uncommon and often include potentially confounding factors, such as a lack of knowledge of predator identity and behavior. We tested how bird behavior influences the survival of three coexisting morphs of the aposematic wood tiger moth Arctia plantaginis offered to a sympatric predator (great tit Parus major) at different frequencies. We found that although positive frequency-dependent selection is present, its strength is affected by predator characteristics and varying prey profitability. These results highlight the need to understand predator foraging in natural communities with variable prey defenses in order to better examine how behavioral interactions shape evolutionary outcomes.Peer reviewe

Geographic mosaic of selection by avian predators on hindwing warning colour in a polymorphic aposematic moth

Warning signals are predicted to develop signal monomorphism via positive frequency-dependent selection (+FDS) albeit many aposematic systems exhibit signal polymorphism. To understand this mismatch, we conducted a large-scale predation experiment in four countries, among which the frequencies of hindwing warning coloration of the aposematic moth,Arctia plantaginis,differ. Here we show that selection by avian predators on warning colour is predicted by local morph frequency and predator community composition. We found +FDS to be the strongest in monomorphic Scotland and lowest in polymorphic Finland, where the attack risk of moth morphs depended on the local avian community. +FDS was also found where the predator community was the least diverse (Georgia), whereas in the most diverse avian community (Estonia), hardly any models were attacked. Our results support the idea that spatial variation in predator communities alters the strength or direction of selection on warning signals, thus facilitating a geographic mosaic of selection.Peer reviewe

Experimental reduction of intromittent organ length reduces male reproductive success in a bug

It is now clear in many species that male and female genital evolution has been shaped by sexual selection. However, it has historically been difficult to confirm correlations between morphology and fitness, as genital traits are complex and manipulation tends to impair function significantly. In this study, we investigate the functional morphology of the elongate male intromittent organ (or processus) of the seed bug Lygaeus simulans, in two ways. We first use micro-computed tomography (micro-CT) and flash-freezing to reconstruct in high resolution the interaction between the male intromittent organ and the female internal reproductive anatomy during mating. We successfully trace the path of the male processus inside the female reproductive tract. We then confirm that male processus length influences sperm transfer by experimental ablation and show that males with shortened processi have significantly reduced post-copulatory reproductive success. Importantly, male insemination function is not affected by this manipulation per se. We thus present rare, direct experimental evidence that an internal genital trait functions to increase reproductive success and show that, with appropriate staining, micro-CT is an excellent tool for investigating the functional morphology of insect genitalia during copulation

Multimodal Aposematic Signals and Their Emerging Role in Mate Attraction

Chemically defended animals often display conspicuous color patterns that predators learn to associate with their unprofitability and subsequently avoid. Such animals (i.e., aposematic), deter predators by stimulating their visual and chemical sensory channels. Hence, aposematism is considered to be "multimodal." The evolution of warning signals (and to a lesser degree their accompanying chemical defenses) is fundamentally linked to natural selection by predators. Lately, however, increasing evidence also points to a role of sexual selection shaping warning signal evolution. One of the species in which this has been shown is the wood tiger moth, Arctia plantaginis, which we here put forward as a promising model to investigate multimodality in aposematic and sexual signaling. A. plantaginis is an aposematic diurnal moth which exhibits sexually dimorphic coloration as well as sex-limited polymorphism in part of its range. The anti-predator function of its coloration and, more recently, its chemical defenses (even when experimentally decoupled from the visual signals), has been well-demonstrated. Interestingly, recent studies have revealed differences between the two male morphs in mating success, suggesting a role of coloration in mate choice or attraction, and providing a possible explanation for its sexual dimorphism in coloration. Here, we: (1) review the lines of evidence showing the role of predation pressure and sexual selection in the evolution of multimodal aposematic signals in general, and in the wood tiger moth in particular; (2) establish gaps in current research linking sexual selection and predation as selective pressures on aposematic signals by reviewing a sample of the literature published in the last 30 years; (3) highlight the need of identifying suitable systems to address simultaneously the effect of natural and sexual selection on multimodal aposematic signals; and (4) propose directions for future research to test how aposematic signals can evolve under natural and sexual selection.Peer reviewe

The causes and consequences of reproductive interference in the Lygaeidae

Electronic version excludes material for which permission has not been granted by the rights holderReproductive interference occurs when individuals direct sexual behaviours towards other species and this causes a reduction in the fitness of one or both of the participants. While initially considered to be little more than an aberration, reproductive interference is increasingly recognised, not just as a factor in determining species co-existence and community dynamics, but also as an opportunity to further our understanding of sexual selection. In this thesis I investigate the causes and consequences of reproductive interference between several species of true bugs (Order: Hemiptera) in the family Lygaeidae. These species have a polygynandrous mating system, in which both males and females mate multiple times. I found that the interspecific mating attempts often witnessed in these bugs is likely a consequence of this mating system, as potential cues for species discrimination, in the form of cuticular hydrocarbons, are available and can be utilised by the bugs in some contexts. This is further supported by the finding that pre-copulatory selection on factors such as diet and chemical protection are weak in these insects. Furthermore, my work highlights the context-dependant nature of both the fitness costs associated with reproductive interference, and also of the bugs’ intra-specific behaviour. When housed in groups, female Lygaeus equestris did not show consistent fitness losses in response to harassment by either conspecific or heterospecific males, despite previous evidence showing that such males inflict costs on both egg production and longevity when interacting one-to-one. This, combined with the finding that male L. equestris alter their mate-guarding behaviour in the presence of other males, highlights the potential of behavioural flexibility to influence the outcome of inter-species interactions, and the importance of context when attempting to measure phenomena such as reproductive interference

Mate-guarding in a promiscuous insect : species discrimination influences context-dependent behaviour

Funding: NERC studentshipMating strategy is often informed by social context. However, information on social environment may be sensitive to interference by nearby heterospecifics, a process known as reproductive interference (RI). When heterospecific individuals are present in the environment, failures in species discrimination can lead to sub-optimal mating behaviours, such as misplaced courtship, misplaced rivalry behaviours, or heterospecific copulation attempts. All aspects of mating behaviour that are influenced by social context may be prone to RI, including copulatory behaviours associated with mate-guarding in the presence of possible competitors. Here we investigate the effect of three heterospecifics on the mate-guarding behaviour of male Lygaeus equestris seed bugs. We find that, despite previously reported heterospecific mating harassment amongst these species of lygaeid bug, male L. equestris are able to effectively distinguish rival conspecific males from heterospecifics. Thus, heterospecific mating attempts in this group may reflect selection on males to mate opportunistically, rather than a failure of species discrimination.Publisher PDFPeer reviewe

The extent and costs of reproductive interference among four species of true bug

ERB-S is supported by a Natural Environment Research Council (NERC) studentship and DMS was in part supported by a NERC Advanced Fellowship.Reproductive interference arises when individuals of one species engage in reproductive activities with individuals of another, leading to fitness costs in one or both species. Reproductive interference (RI) therefore has two components. First, there must be mis-directed mating interactions. Second, there must be costs associated with these mis-directed interactions. Here we consider RI between four species of true bug in the family Lygaeidae, focusing in particular on the fitness consequences to Lygaeus equestris. The species we consider vary in their relationships with each other, including species in the same or different genus, and with or without natural overlap in their geographic ranges. First we show that inter-specific mating interactions, although not a certain outcome, are common enough to perhaps influence mating behaviour in these species (arising in up to 10 % of inter-specific pairings). Second, we show that reproductive interference can seriously reduce female fitness in L. equestris. Importantly, different species impose different costs of RI on L. equestris, with interactions with male Spilostethus pandurus inflicting fitness costs of similar magnitude to the costs of mating with con-specifics. On the other hand, mating interactions with male Oncopeltus fasciatus appear to have no effect on female fitness. In a follow-up experiment, when we allowed competition amongst just females of S. pandurus and L. equestris, the fitness of the latter was not reduced, arguing more strongly for the role of reproductive interference. However, in our final experiments under mass mating conditions with extended ecological interactions (including scope for competition for resources and cannibalism), the costs of RI were less apparent. Our data therefore suggest that the costs of RI will be context-specific and may act in concert with, or be swamped by, other ecological effects. We suggest that comparative studies of this sort that both mimic naturally occurring reproductive interference events, and also artificially generate new ones, will be necessary if we are to better understand the ecological and evolutionary significance of reproductive interference.Publisher PDFPeer reviewe