Different patterns of sperm precedence are expected to entail different costs and benefits of mating for each sex that translate into distinct predictions regarding mating system evolution. Still, most studies addressing these costs and benefits have focused on species with mixed paternity or last male precedence, neglecting first‐male sperm precedence. We attempted to understand whether this latter pattern of sperm precedence translates into different costs and benefits for each sex in the haplodiploid spider mite Tetranychus urticae, a species in which female multiple mating is prevalent but most offspring are sired by first males. First, we assessed the stability of the sperm precedence pattern. To do so, we measured offspring paternity after exposing females to a different number of matings and mating intervals. Next, to determine the potential costs or benefits of multiple mating for females under different contexts, we measured the fecundity and survival of females that re‐mated at different time points. To measure the potential costs of multiple mating for males, we analysed male survival in the presence of different numbers of virgin or mated females. We also tested whether males can reduce offspring production of their competitors, by reducing the production of fertilized offspring of mated females. We found no change in the pattern of sperm precedence, independently of the mating interval between matings and the number of matings. Females paid a cost of mating, as multiply‐mated females laid fewer eggs than once‐mated females. However, while males had reduced survival when exposed to an intermediate number of virgin females, they paid no additional costs of mating with mated females. Moreover, females that mated multiple times produced fewer fertilized offspring than females that mated once. Thus, males that copulated with mated females reduced the fitness of other males, potentially leading to a relative fitness benefit for themselves. Our results show that complex costs and benefits may arise in males in species with first‐male sperm precedence. How these costs and benefits affect the maintenance of selection for polyandry remains an open question.
Symbioses between animals and microbes are ubiquitous, and often have drastic fitness effects on both parties. A rapidly growing body of research now shows that many of these effects are driven by social interactions among the symbionts. For instance, microbes frequently cooperate by producing shareable "public goods" that can mediate both virulence and host-beneficial functions. Conversely, hosts often exert control over symbionts by targeting their social interactions. Despite this pivotal role, we have only started to uncover the full diversity of microbial interactions, and many of the factors that shape variation in their effects on host function and evolution across different symbioses remain elusive. Here, we (i) review the known diversity of microbial interactions across different symbioses, and (ii) argue that variation in their nature and impact is often determined by differences in symbiont diversity. In particular, we first give a primer on the social lives of microbes, and then discuss how intraspecific and interspecific interactions among microbial symbionts affect -and are affected by -their host. Subsequently, we move to the evolution of symbiosis, and discuss the role of microbial interactions in symbioses that feature only few versus many different symbiont species. We show that symbiont-rich symbioses are shaped by strong interspecific competition, which selects against many host-beneficial forms of microbial cooperation, and thereby limits the scope for the evolution of strong host-symbiont dependencies. Conversely, symbioses involving only few symbiont species are often characterized by forms of microbial cooperation that mediate host-beneficial services, a situation that increases the scope for the evolution of host-symbiont dependencies. Overall, we infer that the explicit consideration of social dynamics within symbiont communities of varying complexity is crucial to advance our understanding of how microbes shape animal function and evolution.
The choice of the partner an individual will mate with is expected to strongly impact its fitness. Hence, natural selection has favoured the evolution of cues to distinguish among mates that will provide different fitness benefits to the individual that is choosing. In species with first-male sperm precedence, this is particularly important for males, as mating with mated females will result in no offspring. In the spider mite Tetranychus urticae only the first mating is effective, except if the interval between first and second copulations is shorter than 24 h. In line with this, males prefer to mate with virgin over mated females. They do not, however, choose between females that have mated at different time intervals. Here, we tested which type of cues males use to distinguish between females with different mating status (virgin versus mated). To do so, we firstly confirmed that males prefer virgins over mated females and that they do not select females on the basis of their age or mating interval. Next, we tested whether contact and volatile compounds or chemical trails affected male discrimination between mated and virgin females, by systematically varying the exposure of males to these cues. We found that volatile compounds and chemical trails were sufficient to induce discrimination between virgin and mated females in males. Direct contact with females, however, does not seem to play a role in this discrimination. The composition of such chemical cues (trails and volatiles) remains to be identified.
Microbial invasions can compromise ecosystem services and spur dysbiosis and disease in hosts. Nevertheless, the mechanisms determining invasion outcomes often remain unclear. Here, we examine the role of iron‐scavenging siderophores in driving invasions of Pseudomonas aeruginosa into resident communities of environmental pseudomonads. Siderophores can be ‘public goods’ by delivering iron to individuals possessing matching receptors; but they can also be ‘public bads’ by withholding iron from competitors lacking these receptors. Accordingly, siderophores should either promote or impede invasion, depending on their effects on invader and resident growth. Using supernatant feeding and invasion assays, we show that invasion success indeed increased when the invader could use its siderophores to inhibit (public bad) rather than stimulate (public good) resident growth. Conversely, invasion success decreased the more the invader was inhibited by the residents’ siderophores. Our findings identify siderophores as a major driver of invasion dynamics in bacterial communities under iron‐limited conditions.
Bacteria often cooperate by secreting molecules that can be shared as public goods between cells. Because the production of public goods is subject to cheating by mutants that exploit the good without contributing to it, there has been great interest in elucidating the evolutionary forces that maintain cooperation. However, little is known about how bacterial cooperation evolves under conditions where cheating is unlikely to be of importance. Here we use experimental evolution to follow changes in the production of a model public good, the iron‐scavenging siderophore pyoverdine, of the bacterium Pseudomonas aeruginosa. After 1200 generations of evolution in nine different environments, we observed that cheaters only reached high frequency in liquid medium with low iron availability. Conversely, when adding iron to reduce the cost of producing pyoverdine, we observed selection for pyoverdine hyperproducers. Similarly, hyperproducers also spread in populations evolved in highly viscous media, where relatedness between interacting individuals is increased. Whole‐genome sequencing of evolved clones revealed that hyperproduction is associated with mutations involving genes encoding quorum‐sensing communication systems, while cheater clones had mutations in the iron‐starvation sigma factor or in pyoverdine biosynthesis genes. Our findings demonstrate that bacterial social traits can evolve rapidly in divergent directions, with particularly strong selection for increased levels of cooperation occurring in environments where individual dispersal is reduced, as predicted by social evolution theory. Moreover, we establish a regulatory link between pyoverdine production and quorum‐sensing, showing that increased cooperation with respect to one trait (pyoverdine) can be associated with the loss (quorum‐sensing) of another social trait.
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