Dynamic rodent behavioral response to predation risk: implications for disease ecology.

Prey modify their behavior in response to variation in predation risk, and such modifications can affect trophic processes such as disease transmission. However, variation in predation risk is complex, arising from direct risk from the predator itself and indirect risk due to the environment. Moreover, direct risk typically stems from multiple predators and varies over timescales (e.g., a predator nearby vs. its seasonal activities). We implemented a field-based experiment to disentangle these sources of risk and relate them to antipredator behavior in rodents. We modeled rodent occurrence and activity as a function of short- and long-term risk from a primary predator, red foxes (Vulpes vulpes), long-term risk from a second predator, coyotes (Canis latrans), and environmental variables. We found that long-term red fox activity strongly reduced rodent occurrence and that cues of nearby red fox presence decreased rodent activity by > 50%. In addition, this activity reduction was dynamic in that varied according to the background level of long-term red fox activity. Importantly, rodents did not respond to environmental variables (moonlight, temperature, and habitat) or long-term coyote activity. These results bear upon recent work that suggests predators can alter tick-borne disease dynamics via induced antipredator behavior of rodents, which are hosts for pathogens and ticks. Specifically, our study corroborates the hypothesis that red foxes act as important proximal agents in regulating tick-borne diseases by reducing rodent activity. More generally, this study highlights the need to consider the dynamic nature of prey antipredator response across landscapes with variable long-term predation risk.

Insect behaviour: migratory bands give crickets protection.

Mormon crickets and juvenile locusts form huge migratory bands--millions of individuals march in unison across the landscape and devastate vast agricultural areas, but little is known about why these bands form. Here we use radiotelemetry to show that band membership benefits these insects by greatly reducing the probability that they will become victims of predators. It is likely that migratory banding has evolved because it gives substantial protection to individuals within the group.

Loss of safety in numbers and a novel driver of mass migration: radiotelemetry reveals heavy wasp predation on a band of Mormon crickets.

Coordinated movement of animals is a spectacular phenomenon that has received much attention. Experimental studies of Mormon crickets and locust nymphs have demonstrated that collective motion can arise from cannibalism that compensates for nutritional deficiencies arising from group living. Grouping into migratory bands confers protection from predators. By radiotracking migrating, Mormon crickets released over 3 days, we found that specialized, parasitoid digger wasps (Sphecidae) respond numerically and prey heavily on aggregated Mormon crickets leading to loss of safety in numbers. Palmodes laeviventris paralysed and buried 42% of tagged females and 8% of the males on the final day of tracking. Risk of wasps and Mormon crickets hatching on the same site is high and may drive nymphal emigration. A preference to provision offspring with adult female Mormon crickets can be explained by their greater fat content and larger size compared with males, improving survival of wasps during diapause.

Postmating-prezygotic isolation is not an important source of selection for reinforcement within and between species in Drosophila pseudoobscura and D. persimilis.

Most work on adaptive speciation to date has focused on the role of low hybrid fitness as the force driving reinforcement (the evolution of premating isolation after secondary contact that reduces the likelihood of matings between populations). However, recent theoretical work has shown that postmating, prezygotic incompatibilities may also be important in driving premating isolation. We quantified premating, postmating-prezygotic, and early postzygotic fitness effects in crosses among three populations: Drosophila persimilis, D. pseudoobscura USA (sympatric to D. persimilis), and D. pseudoobscura Bogotá (allopatric to D. persimilis). Interspecific matings were more likely to fail when they involved the sympatric populations than when they involved the allopatric populations, consistent with reinforcement. We also found that failure rate in sympatric mating trials depended on whether D. persimilis females were paired with D. pseudoobscura males or the reverse. This asymmetry most likely indicates differences in discrimination against heterospecific males by females. By measuring egg laying rate, fertilization success and hatching success, we also compared components of postmating-prezygotic and early postzygotic isolation. Postmating-prezygotic fitness costs were small and not distinguishable between hetero- and conspecific crosses. Early postzygotic fitness effects due to hatching success differences were also small in between-population crosses. There was, however, a postzygotic fitness effect that may have resulted from an X-linked allele found in one of the two strains of D. pseudoobscura USA. We conclude that the postmating-prezygotic fitness costs we measured probably did not drive premating isolation in these species. Premating isolation is most likely driven in sympatric populations by previously known hybrid male sterility.

Understanding reversals in the relative strength of sexual selection on males and females: a role for sperm competition?

Sperm competition affects sexual selection intensity on males, but models suggest it cannot affect the relative intensity of sexual selection on males compared to females. However, if sperm competition depresses the payoff for male multiple mating, it could affect the relative intensity of sexual selection and even cause sexual selection to be more intense on females than males (reversal of typical pattern). To evaluate how sperm competition, energy availability, and parental investment affect the intensity of sexual selection on each sex, I constructed a simulation model using the relationship between fecundity and number of mates to estimate sexual selection gradients. Unlike earlier models, I include a trade-off between paternal investment and sperm competition ability. The amount of energy available for reproduction affects the sexual selection gradient for each sex. Reversals in the sex experiencing stronger sexual selection do occur when additional paternal investment reduces a male's ability to compete for fertilizations within females. The shape of the distribution of mates for each sex (determined by mate competition) is also important. Output from the model is qualitatively similar to empirical data from insects with paternal investment. This model challenges previous thinking about the role of sperm competition in sex-role reversal.

Coping with uncertainty: nutrient deficiencies motivate insect migration at a cost to immunity.

Migration often is associated with movement away from areas with depleted nutrients or other resources, and yet migration itself is energetically demanding. Migrating Mormon crickets Anabrus simplex (Orthoptera: Tettigoniidae) lack nutrients, and supplementation of deficient nutrients slows migratory movements and enhances specific aspects of their immune systems. Migrants deficient in proteins have less spontaneous phenoloxidase (PO) activity, whereas those deficient in carbohydrates have lower lysozyme-like anti-bacterial titers with a proposed compromise between migratory and anti-bacterial activities. To investigate the relationship between diet, movement, and immunity further, we removed Mormon crickets from a migratory band and offered each cricket one of five diets: high protein, high carbohydrate, equal weight of proteins and carbohydrates (P + C), vitamins only, or water only for 1 h. We then attached a radio, returned each to the migratory band, and recaptured them 18-24 h later. Mormon crickets fed protein moved the furthest, those with only water or only vitamins moved less, and those fed carbohydrates or P + C moved the least. Standard intake trials also indicated that the Mormon crickets were deficient in carbohydrates. Consistent with a previous study, lysozyme-like anti-bacterial activity was greatest in those fed carbohydrates, and there was no difference between those fed water, protein, or P + C. Crickets were removed from the same migratory band and fed one of four diets: high P, high C, P + C, or vitamins only, for 1 h. Then the crickets were held in captivity with water only for 4 or 24 h before blood was drawn. Immunity measures did not differ between times of draw. Diet treatments had no effect on anti-bacterial activity of captive Mormon crickets, whereas total PO was greater in those fed protein. These results support the hypothesis of a direct compromise between migratory and anti-bacterial activities, whereas PO is compromised by low protein independent of migratory activities. We discuss the potential effects of climate on nutritional deficits and susceptibility to different pathogens.

The social context of cannibalism in migratory bands of the Mormon cricket.

Cannibalism has been shown to be important to the collective motion of mass migratory bands of insects, such as locusts and Mormon crickets. These mobile groups consist of millions of individuals and are highly destructive to vegetation. Individuals move in response to attacks from approaching conspecifics and bite those ahead, resulting in further movement and encounters with others. Despite the importance of cannibalism, the way in which individuals make attack decisions and how the social context affects these cannibalistic interactions is unknown. This can be understood by examining the decisions made by individuals in response to others. We performed a field investigation which shows that adult Mormon crickets were more likely to approach and attack a stationary cricket that was side-on to the flow than either head- or abdomen-on, suggesting that individuals could reduce their risk of an attack by aligning with neighbours. We found strong social effects on cannibalistic behaviour: encounters lasted longer, were more likely to result in an attack, and attacks were more likely to be successful if other individuals were present around a stationary individual. This local aggregation appears to be driven by positive feedback whereby the presence of individuals attracts others, which can lead to further crowding. This work improves our understanding of the local social dynamics driving migratory band formation, maintenance and movement at the population level.

Cannibal crickets on a forced march for protein and salt.

Swarming and mass migration are spectacular and sometimes devastating features of the biology of various animal species. These phenomena are typically associated with actual or anticipated depletion of food resources after an increase in population density, but the mechanisms driving such collective movements are poorly understood. Here we reveal that insects in large, coordinated migratory bands consisting of millions of Mormon crickets in western North America were deprived of two essential nutritional resources: protein and salt. The insects themselves provided a major source of these nutrients, and cannibalism was rife. We show that protein and salt satiation reduced cannibalism and that protein satiation inhibited walking. Additionally, experimentally reducing the motility or mobility of crickets substantially increased their risk of being cannibalized by other band members. As a result, the availability of protein and salt in the habitat will influence the extent to which bands march, both through the direct effect of nutrient state on locomotion and indirectly through the threat of cannibalism by resource-deprived crickets approaching from the rear. The crickets are, in effect, on a forced march. Migratory band formation and subsequent mass movement, therefore, are manifestations of specific tradeoffs between the costs and benefits of group living. Bands afford antipredator benefits to individual group members. Group movement then mitigates the resulting costs of intraspecific competition, namely local depletion of nutritional resources and the associated increased risk of cannibalism.

Using upper limits of "bateman gradients" to estimate the opportunity for sexual selection.

The widespread use of molecular markers to estimate parentage makes possible a new index of the opportunity for sexual selection. After demonstrating the need for a new measure, I develop one based on the upper limit on sexual selection. I describe what sets the upper limit for each sex by showing how maximum fecundity increases with number of mates, accounting for the amount of energy (or critical resources) available for reproduction and levels of parental care. For females the upper limit on sexual selection is set by the value of paternal investment that comes with each mating. For males, the upper limit on sexual selection is set by the fecundity of their mates (including any boost to female fecundity from paternal investment). Sex-roles are most likely to reverse (making males choosy and females competitive) when the amount of reproductive energy investment made by each sex is low, irrespective of the level of paternal investment. Finally, I propose that we use the difference between male and female upper limits on sexual selection to quantify sex differences in the opportunity for sexual selection. Using upper limits to estimate the opportunity for sexual selection is more intuitive than older methods (e.g., standardized variance in mating success), it is experimentally measurable, and it is valuable in understanding the evolution of mating systems.

Sex differences in recombination and mapping adaptations.

Since the raw material of marker based mapping is recombination, understanding how and why recombination rates evolve, and how we can use variation in these rates will ultimately help to improve map resolution. For example, using this variation could help in discriminating between linkage and pleiotropy when QTL for several traits co-locate. It might also be used to improve QTL mapping algorithms. The goals of this chapter are: (1) to highlight differences in recombination rates between the sexes, (2) describe why we might expect these differences, and (3) explore how sex difference in recombination can be used to improve resolution in QTL mapping.