Daniel González-Tokman

Mating success and energetic condition effects driven by terminal investment in territorial males of a short‐lived invertebrate

Summary The terminal investment hypothesis has two predictions: in the face of an infection (i) mature males will increase investment to traits that increase mating success, while such investments will occur to a less extent in young males; and (ii) physiological costs of resource reallocation will be more severe for infected mature males than for infected young males. Although these predictions have been tested in long-lived vertebrates, prior studies have not examined actual resource allocation conflicts. Here, we have tested the above predictions and have investigated the energetic costs of increased mating by old males, using a short-lived invertebrate, the damselfly Hetaerina americana. Males of this species defend territories as the main way to obtain access to females. Using groups of infected vs. noninfected males of two different ages, we found that compared to young infected males, mature infected males defended territories for longer, had higher mating success and directed agonistic behaviour to conspecific males more frequently. Despite similar immune responses by mature and young males, infected mature males ended up with less fat reserves compared to infected young males. This suggests that resource allocation conflicts are more severe for mature than for young males. In general, these results suggest that the terminal investment hypothesis applies in males of short-lived invertebrates and that a cause of increased mating success for males of advanced ages is reduced energetic stores.

Infection effects on feeding and territorial behaviour in a predatory insect in the wild

Sick animals may change their feeding behaviour to compensate for infections. However, there is little information regarding whether infection affects (1) feeding behaviour of predators, (2) feeding behaviour using an experimental approach in the wild, (3) other costly behaviours and/or (4) physiological components of condition. We experimentally infected males of the predatory damselfly Hetaerina americana in a field experiment. We hypothesized that infection would reduce feeding behaviour. We further predicted a reduction in territorial activity, an increase in immune response (measured by the activity of phenoloxidase, PO) and a reduction of fat reserves and flight-associated muscle mass (two traits usually traded off with immune ability and territorial behaviour). We also infected males in a laboratory experiment that controlled for food supply and territorial activity, and measured the same physiological characters. Immune challenges in the field experiment unexpectedly increased feeding rate but did not change territorial activities. Muscle mass was reduced in the field but not in the laboratory, probably because of differences in the presence of energetically expensive territorial activities. In the laboratory, starvation and infection reduced PO activity and fat stores but did not affect muscle mass. Thus, our field and laboratory results support the idea that increased feeding compensates for infections in predators.

Territorial damselflies do not show immunological priming in the wild

Adaptive immunity allows vertebrates to gain protection against repeated pathogenic infections. Analogous responses (priming) have been recently uncovered in invertebrates. However, whether such responses are widespread is not known. The present study investigated the presence of immunological priming in males of a species whose phylogenetic position places it in one of the less derived insect orders. It is hypothesized that the efficiency of such a response could be related to animal condition, as assessed by the expression of a sexually selected ornament. Hetaerina americana Fabricius (Odonata: Calopterygidae) males bear a conspicuous ornament (a red wing spot), which is evolutionarily maintained via male territorial competition. Using field‐collected animals, a group of males is challenged with bacteria before exposure to a higher dose of the same or a different bacteria, and survival is compared with that of infected males not previously challenged, as well as control groups. Gram‐positive and Gram‐negative bacteria are used. To explore how long priming may take to work, the second exposure is carried out either after 1 or 5 days. Red spot and body size are entered in the analysis as predictors of survival within and between groups. There is no difference in survival among groups, which suggests no priming effect. Overall, red spot and body size are not consistent in explaining survival.

Support for the immunocompetence handicap hypothesis in the wild: hormonal manipulation decreases survival in sick damselflies.

The immunocompetence handicap hypothesis (ICHH) states that hormones enhance sexual trait expression but impair immunity. Previous tests of the ICHH have been hampered by experimental design problems. Here, we report on an experimental test of the ICHH that includes manipulations of both hormones and infections in males of the territorial damselfly, Hetaerina americana, with accurate survival measurements. We conducted a fully factorial experiment subjecting each individual to one of three topical treatments: methoprene (a juvenile hormone analog), acetone, or control, and one of three injection treatments: bacteria, PBS, or control. We measured survival of manipulated males in both the wild and in captivity. As predicted, survival was most heavily impaired in methoprene‐bacteria males than in the other groups in the wild, and no survival differences emerged in captive animals. This result confirms that survival is one cost an animal pays for increased hormonal levels. This corroborates theoretical predictions of the ICHH.

Survival after experimental manipulation in the territorial damselfly Hetaerina titia (Odonata: Calopterygidae): more ornamented males are not more pathogen resistant

It has been hypothesized that sexual ornaments communicate pathogen resistance ability. We experimentally explored the relationship between the expression of a male ornamental trait (wing pigmentation) of the damselfly Hetaerina titia and survival after a bacterial challenge. We infected males with Serratia marcescens (a Gram-negative bacteria typical of insects) and compared survival against a group infected with dead bacteria and a noninfected group. Wing pigmentation was entered as a predictor of survival in this comparison. Our study indicated that wing pigmentation was not a good predictor of immune ability against bacteria. This result contradicts previous findings in the same and other calopterygid species in which wing pigmentation intensity inversely correlated with gregarine infection levels. It also contradicts the general idea that ornaments are honest indicators of pathogen defense.

A Mismatch between the Perceived Fighting Signal and Fighting Ability Reveals Survival and Physiological Costs for Bearers

Signals of fighting indicate an animals intention to attack and so they serve to prevent costly aggressive encounters. However, according to theory, a signal that is different in design (i.e. a novel signal) but that fails to inform fighting intentions will result in negative fitness consequences for the bearer. In the present study we used males of the territorial damselfly Hetaerina americana, which have a red wing spot during territory defense that has evolved as a signal of fighting ability. By producing a novel signal (covering the red spot with blue ink) in territory owners, we investigated: a) the behavioral responses by conspecific males; b) survival cost and c) three physiological mediators of impaired survival: muscular fat reserves, muscle mass and immune ability. We predicted that males with the novel signal would be attacked more often by conspecifics as the former would fail to convey fighting ability and intentions adequately. This will result in lower survival and physiological condition for the novel signal bearers. We found that, compared to control males (males whose red spot was not changed), experimental males had reduced survival, were less able to hold a territory, and had a reduced muscle mass. It seems that spot modified males were not able to effectively communicate their territory tenancy, which may explain why they lost their defended sites. Our results provide support for theoretical models that a novel signal that fails to informing fighting ability may lead to a fitness cost for bearers.

Effect of juvenile hormone analog in a natural host-parasite system

Hormones mediate the physiological responses of animals to environmental changes. Consequently, hormones can be responsible of trade offs between different life history traits. Juvenile hormone (JH) is thought to mediate resource allocation in insects: specifically, it is thought to enhance the expression of condition-related traits like sexual signals, whilst reducing immune responsiveness. Here, we experimentally test whether a JH analog (JHa) had an effect on immunity of male dragonflies Celithemis eponina, and if such effects are translated into faster growth or development of a natural parasite (water mite). We also tested the effects of JHa on host condition (muscular mass and fat reserves) of mature male dragonflies. Mites from JHa treated dragonflies grew faster than mites from control dragonflies receiving just an acetone carrier. However, there was no effect of JHa on measures of host immune response (melanization of a nylon implant) or condition of mature males. We suggest that better parasite growth in JHa treated males does not result from the JH immunosuppressive function, but instead it appears that parasites receive hormone signals from the host and alter their development without affecting host condition measurably. Our work highlights the importance of measuring both immune parameters and response to real parasites when studying evolutionary trade offs.

Effect of juvenile hormone on senescence in males with terminal investment

Senescence, a decline in survival and reproductive prospects with age, is controlled by hormones. In insects, juvenile hormone (JH) is involved in senescence with captive individuals, but its effect under natural conditions is unknown. We have addressed this gap by increasing JH levels in young and old wild males of the damselfly Hetaerina americana. We assessed survival in males that were treated with a JH analogue (methoprene), which is known to promote sexual activity, and an immune challenge, which is known to promote terminal investment in reproduction in the studied species. We replicated the same procedure in captivity (to control for environmental variation), where males were deprived of any activity or food. We expected old males to show the lowest survival after being treated with JH and immune‐challenged, because the effect of terminal investment on senescence would be exacerbated by JH. However, this should be the case for wild animals, but not for captive animals, as the effects of JH and immune challenge should lead to an increase in high energetic‐demanding activities only occurring in the wild. Old animals died sooner compared with young animals in both the wild and captivity, confirming that males are subject to senescence. In wild but not captive animals, JH decreased survival in young males and increased it in old males, confirming that JH is sensitive to the environment when shaping animal senescence. Immune challenge had no effect on survival, suggesting no effect of terminal investment on senescence. Additionally, contrary to the expected effects of terminal investment, with an immune challenge, recapture rates increased in young males and decreased in old males. Our results show that male senescence in the wild is mediated by JH and that terminal investment does not cause senescence. One explanation is that animals undergoing senescence and terminal investment modify their feeding behaviour to compensate for their physiological state.

Effects of an herbicide on physiology, morphology, and fitness of the dung beetle Euoniticellus intermedius (Coleoptera: Scarabaeidae)

Some agrochemical compounds threaten nontarget organisms and their functions in the ecosystem. The authors experimentally evaluated the effects of one of the most common herbicide mixtures used worldwide, containing 2,4-dichlorophenoxyacetic acid and picloram, on dung beetles, which play fundamental roles in the function of natural and managed ecosystems. The present study employed techniques of physiology and geometric morphometrics, besides including fitness measurements, to assess the effects of the herbicide in the introduced beetle Euoniticellus intermedius. Because herbicide components promote oxidative stress and affect survival in certain insects, the authors predicted negative effects on the beetles. Unexpectedly, no effect of herbicide concentration was found on clutch size, sex ratio, and fluctuating asymmetry, and it even increased physiological condition and body size in exposed beetles. Because the studied species presents 2 male morphs, the authors, for the first time, evaluated the effect of a pollutant on the ratio of these morphs. Contrary to the prediction, the herbicide mixture increased the proportion of major males. Thus, the herbicide does not threaten populations of the studied beetles. The present study discusses how both negative and positive effects of pollutants on wild animals modify natural and sexual selection processes occurring in nature, which ultimately impact population dynamics. The authors recommend the use of physiological and geometric morphometrics techniques to assess the impact of pollutants on nontarget animals. Environ Toxicol Chem 2017;36:96-102.

Allometry of Male Grasping Apparatus in Odonates Does Not Suggest Physical Coercion of Females

Male abdominal grasping apparatus that are used to secure a female prior, during and after mating, are widespread in arthropods. The scarce evidence regarding its selective regime suggests that they are male adaptations to circumvent female mating decisions, as predicted by the sexual conflict hypothesis. A recent discussion regarding this way of selection suggests that, similar to weapons and traits that have to do with physical endurance, grasping apparatus should show hyperallometry (proportionally larger compared to body size) as an indication of selection towards increased size. We have tested this idea by measuring the length, width and area of the grasping apparatus of five dragonfly species (Anax junius, Rhionaeschna multicolor, Dythemis nigrescens, D. sterilis and Phyllogomphoides pacificus). We used two proxies of body size (wing and body length). Our measures did not indicate any pattern of hyperallometry. Thus, the grasping apparatus in these animals does not seem to be positively selected for increased size as would be expected if they were forcing females to mate. Given this, we discuss three other explanations for the maintenance of the grasping apparatus in odonates: 1) a firm grip that secures the tandem and mating position; 2) courtship devices subject to female choice; and, 3) isolation structures that mechanically prevent interspecific matings. The first hypothesis, however, could not explain the highly elaborated and species specific morphology of grasping apparatus in these animals. Support for the second hypothesis comes from the fact that odonate females have mechanoreceptor sensilla embedded in their mesostigmal plates (the place grabbed by the grasping apparatus). For the third hypothesis, coevolutionary patterns in morphology in the grasping apparatus and mesostigmal plates in some Zygoptera can also be used as support.