Complex battlefields favor strong soldiers over large armies in social animal warfare.

In social animals, success can depend on the outcome of group battles. Theoretical models of warfare predict that group fighting ability is proportional to two key factors: the strength of each soldier in the group and group size. The relative importance of these factors is predicted to vary across environments [F. W. Lanchester, Aircraft in Warfare, the Dawn of the Fourth Arm (1916)]. Here, we provide an empirical validation of the theoretical prediction that open environments should favor superior numbers, whereas complex environments should favor stronger soldiers [R. N. Franks, L. W. Partridge, Anim. Behav. 45, 197-199 (1993)]. We first demonstrate this pattern using simulated battles between relatively strong and weak soldiers in a computer-driven algorithm. We then validate this result in real animals using an ant model system: In battles in which the number of strong native meat ant Iridomyrmex purpureus workers is constant while the number of weak non-native invasive Argentine ant Linepithema humile workers increases across treatments, fatalities of I. purpureus are lower in complex than in simple arenas. Our results provide controlled experimental evidence that investing in stronger soldiers is more effective in complex environments. This is a significant advance in the empirical study of nonhuman warfare and is important for understanding the competitive balance among native and non-native invasive ant species.

Kin-mediated plasticity in alternative reproductive tactics.

Conditional strategies occur when the relative fitness pay-off from expressing a given phenotype is contingent upon environmental circumstances. This conditional strategy model underlies cases of alternative reproductive tactics, in which individuals of one sex employ different means to obtain reproduction. How kin structure affects the expression of alternative reproductive tactics remains unexplored. We address this using the mite Rhizoglyphus echinopus, in which large males develop into aggressive 'fighters' and small males develop into non-aggressive 'scramblers.' Because only fighters kill their rivals, they should incur a greater indirect fitness cost when competing with their relatives, and thus fighter expression could be reduced in the presence of relatives. We raised mites in full-sibling or mixed-sibship groups and found that fighters were more common at higher body weights in full-sibling groups, not less common as we predicted (small individuals were almost exclusively scramblers in both treatments). This result could be explained if relatedness and cue variability are interpreted signals of population density, since fighters are more common at low densities in this species. Alternatively, our results may indicate that males compete more intensely with relatives in this species. We provide the first evidence of kin-mediated plasticity in the expression of alternative reproductive tactics.

Fish out of water: Aquatic parasites in a drying world.

Although freshwater ecosystems are among the most diverse and endangered in the world, little attention has been paid to either the importance of parasitic disease as a threatening process for freshwater organisms, or the co-extinction risk of freshwater parasites. In this review, we use theoretical and empirical studies of host/parasite interactions to examine these issues, particularly with respect to the threat posed by climate change to fish and parasite communities in intermittent rivers. Intermittent rivers are those that cease to flow at any point in time or space, with isolated pools providing ecological refuges for freshwater biota between streamflow events. Intermittent rivers are the dominant river type in arid, semi-arid and Mediterranean regions; areas of the world that have experienced dramatic decreases in streamflow as a result of climate change. Reduced streamflow decreases the number, size and connectivity of refuge pools in intermittent rivers, with important consequences for free-living aquatic organisms, particularly fishes, and their parasitic fauna. As a result of more frequent and sustained periods of no flow, parasite diversity within refuge pools is expected to decrease, with a concomitant increase in the prevalence and intensity of those parasite species which do survive, particularly host generalists. Decreased connectivity between refuge pool communities should increase the spatial modularity of host/parasite interactions, leading to a greater structuring of host and parasite communities along the river. This increases the probability of species loss (for both hosts and their parasites), as local extinctions cannot be reversed by colonisation from other localities.

No evidence for divergence in male harmfulness or female resistance in response to changes in the opportunity for dispersal.

The outcome of sexual conflict can depend on the social environment, as males respond to changes in the inclusive fitness payoffs of harmfulness and harm females less when they compete with familiar relatives. Theoretical models also predict that if limited male dispersal predictably enhances local relatedness while maintaining global competition, kin selection can produce evolutionary divergences in male harmfulness among populations. Experimental tests of these predictions, however, are rare. We assessed rates of dispersal in female and male seed beetles Callosobruchus maculatus, a model species for studies of sexual conflict, in an experimental setting. Females dispersed significantly more often than males, but dispersing males travelled just as far as dispersing females. Next, we used experimental evolution to test whether limiting dispersal allowed the action of kin selection to affect divergence in male harmfulness and female resistance. Populations of C. maculatus were evolved for 20 and 25 generations under one of three dispersal regimens: completely free dispersal, limited dispersal and no dispersal. There was no divergence among treatments in female reproductive tract scarring, ejaculate size, mating behaviour, fitness of experimental females mated to stock males or fitness of stock females mated to experimental males. We suggest that this is likely due to insufficient strength of kin selection rather than a lack of genetic variation or time for selection. Limited dispersal alone is therefore not sufficient for kin selection to reduce male harmfulness in this species, consistent with general predictions that limited dispersal will only allow kin selection if local relatedness is independent of the intensity of competition among kin.

Male responses to sperm competition when rivals vary in number and familiarity.

Males of many species adjust their reproductive investment to the number of rivals present simultaneously. However, few studies have investigated whether males sum previous encounters with rivals, and the total level of competition has never been explicitly separated from social familiarity. Social familiarity can be an important component of kin recognition and has been suggested as a cue that males use to avoid harming females when competing with relatives. Previous work has succeeded in independently manipulating social familiarity and relatedness among rivals, but experimental manipulations of familiarity are confounded with manipulations of the total number of rivals that males encounter. Using the seed beetle Callosobruchus maculatus, we manipulated three factors: familiarity among rival males, the maximum number of rivals encountered simultaneously and the total number of rivals encountered over a 48 h period. Males produced smaller ejaculates when exposed to more rivals in total, regardless of the maximum number of rivals they encountered simultaneously. Males did not respond to familiarity. Our results demonstrate that males of this species can sum the number of rivals encountered over separate days, and therefore the confounding of familiarity with the total level of competition in previous studies should not be ignored.

Dietary antioxidants, but not courtship effort, affect oxidative balance in the testes and muscles of crickets.

Recent interest has focused on the role of reactive oxygen species (ROS) as universal constraints in life-history evolution. Empirical studies have examined the oxidative costs of reproduction for females, with little work conducted on males. The male germline is thought to be particularly susceptible to oxidative damage because the testes, and the sperm themselves, can be prolific producers of ROS. We tested the hypothesis that protection of the male germline from oxidative damage represents a cost of reproduction for males. We fed male crickets, Teleogryllus oceanicus, with one of two experimental diets in which we manipulated the availability of dietary antioxidants, and we induced variation in their expenditure on courtship effort by manipulating access to females. We measured the total antioxidant capacity, levels of ROS production and the amount of oxidative damage to proteins in both testis and thoracic muscle tissues. Dietary antioxidants contributed to positive oxidative balance in both tissue types. Although the testes had greater antioxidant defences than muscle tissue, they also produced considerably higher levels of ROS and sustained higher levels of oxidative damage. Courtship effort had no impact on any measure of oxidative balance. Our data confirm that the male germline is especially susceptible to oxidative stress and that dietary antioxidants can alleviate this oxidative cost of reproduction.

Males harm females less when competing with familiar relatives.

Sexual conflict occurs when reproductive partners have different fitness optima, and can lead to the evolution of traits in one sex that inflict fitness costs on the opposite sex. Recently, it has been proposed that antagonism by males towards females should be reduced when they compete with relatives, because reducing the future productivity of a female would result in an indirect fitness cost for a harmful male. We tested this prediction in the seed beetle Callosobruchus maculatus, the males of which harm females with genital spines and pre-copulatory harassment. We compared lifespan, lifetime egg production and lifetime offspring production among females housed with groups of males that varied in their familiarity and relatedness. Females produced significantly more eggs and offspring when grouped with males who were both related and familiar to each other. There was no effect of male relatedness or familiarity on female lifespan. Our results suggest that males plastically adjust their harmfulness towards females in response to changes in inclusive fitness payoffs, and that in this species both genetic relatedness and social familiarity mediate this effect.

Mutualists or parasites? Context-dependent influence of symbiotic fly larvae on carnivorous investment in the Albany pitcher plant.

Carnivorous plants allocate more resources to carnivorous structures under nutrient-limited conditions, and relative investment can also be influenced by animals (infauna) that live in association with these plants and feed on their prey. We investigated these effects within a population of the pitcher plant Cephalotus follicularis containing varying densities of larvae of the fly Badisis ambulans. For plants with a relatively high proportion of adult pitchers, increasing larval density was associated with lower relative leaf allocation to new pitcher buds. For plants with relatively few adult pitchers, however, there was greater relative leaf allocation to pitcher buds with increasing larval density. In a field experiment, there was no significant effect of experimental larval presence or absence on the change in carbon-to-nitrogen (C/N) ratio of plants. Although the direction of the correlation between B. ambulans larvae and relative investment in carnivorous and non-carnivorous structures depends on the relative number of mature structures, whether the larvae enhance or reduce nutrient stress under different conditions remains unclear. The change in C/N was, however, less variable for pitchers that contained larvae, suggesting a stabilizing effect. Eighteen of 52 experimental pitchers were damaged by an unknown species, causing the pitcher fluid to drain. These pitchers were significantly more likely to survive if they contained larvae. These results suggest that the relationship between infauna and host varies with the initial resource status and environmental context of the host plant.