Roberto Munguía-Steyer

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.

The sicker sex: understanding male biases in parasitic infection, resource allocation and fitness.

The “sicker sex” idea summarizes our knowledge of sex biases in parasite burden and immune ability whereby males fare worse than females. The theoretical basis of this is that because males invest more on mating effort than females, the former pay the costs by having a weaker immune system and thus being more susceptible to parasites. Females, conversely, have a greater parental investment. Here we tested the following: a) whether both sexes differ in their ability to defend against parasites using a natural host-parasite system; b) the differences in resource allocation conflict between mating effort and parental investment traits between sexes; and, c) effect of parasitism on survival for both sexes. We used a number of insect damselfly species as study subjects. For (a), we quantified gregarine and mite parasites, and experimentally manipulated gregarine levels in both sexes during adult ontogeny. For (b), first, we manipulated food during adult ontogeny and recorded thoracic fat gain (a proxy of mating effort) and abdominal weight (a proxy of parental investment) in both sexes. Secondly for (b), we manipulated food and gregarine levels in both sexes when adults were about to become sexually mature, and recorded gregarine number. For (c), we infected male and female adults of different ages and measured their survival. Males consistently showed more parasites than females apparently due to an increased resource allocation to fat production in males. Conversely, females invested more on abdominal weight. These differences were independent of how much food/infecting parasites were provided. The cost of this was that males had more parasites and reduced survival than females. Our results provide a resource allocation mechanism for understanding sexual differences in parasite defense as well as survival consequences for each sex.

Strengthening Population Inference in Herpetofaunal Studies by Addressing Detection Probability

Abstract In conservation biology and population dynamic studies, accounting for the effect of imperfect detection of animals in the wild is crucial for correct inference of demographic parameters. However, articles published in South American herpetological journals still report estimates without considering how detection can influence estimates of vital rates, assuming that detection probability is perfect (i.e., 100%) and constant. Using data from a population of the torrent frog, Hylodes asper, we calculate return rates and compare them with survival probability estimates adjusted for detection probability to highlight the discrepancies between the two metrics. Then, using power analysis, we also explore how survival is underestimated, considering different scenarios and sampling efforts, given low detectability. Finally, we provide information on the optimal number of surveys to achieve a reasonable precision, assuming a fixed number of individuals initially captured for a series of parameter values. Ignoring potential bias of uncorrected estimates may lead to weak inference and erroneous decisions for management and conservation. We recommend that researchers consider detection probability in their studies to improve the accuracy of population estimates.

Population dynamics of the critically endangered golden lancehead pitviper, Bothrops insularis: stability or decline?

Little is known about vital rates of snakes generally because of the difficulty in collecting data. Here we used a robust design mark-recapture model to estimate survival, behavioral effects on capture probability, temporary emigration, abundance and test the hypothesis of population decline in the golden lancehead pitviper, Bothrops insularis, an endemic and critically endangered species from southeastern Brazil. We collected data at irregular intervals over ten occasions from 2002 to 2010. Survival was slightly higher in the wet season than in the dry season. Temporal emigration was high, indicating the importance of accounting for this parameter both in the sampling design and modeling. No behavioral effects were detected on capture probability. We detected an average annual population decrease ( = 0.93, CI = 0.47–1.38) during the study period, but estimates included high uncertainty, and caution in interpretation is needed. We discuss the potential effects of the illegal removal of individuals and the implications of the vital rates obtained for the future persistence and conservation of this endemic, endangered species.

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.

Paternal Care and Sexual Selection in Arthropods

Abstract Exclusive paternal care is probably the rarest form of post-zygotic parental investment in nature. In arthropods, this behavior has independently evolved in 15 lineages, including approximately 1500 species. Here, we review the theoretical background for the evolution of parental investment and sex roles, contrasting classical views with the most recent mathematical models. Then, we introduce cases of exclusive paternal care in arthropods and explore empirical information, focusing on the costs and benefits of male egg guarding and the possible role of paternal care in male attractiveness and sex role reversal. Finally, we analyze the possible effects of temperature and rainfall on several ecological aspects that are likely to influence the evolution and maintenance of paternal care, and also derive specific macroecological predictions to be tested in future studies.

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.

Isometric patterns for male genital allometry in four damselfly species

Recent studies have found that insect genitalic traits show negative allometry, i.e., are relatively small in relation to body size. One interpretation of this is that males use their genitalia to stimulate females. Thus, given the nature of damselfly copulation in which males physically reach the rival sperm that females have stored from previous matings, male genitalic traits are not expected to show negative allometry. To test this idea, we assessed (a) the rival sperm displacement function by the mating male and (b) allometry of aedeagal length of four damselfly species (Argia anceps, Argia tezpi, Argia extranea, and Enallagma praevarum). Sperm displacement was assessed by inspecting whether the aedeagus reached the rival sperm during copulation in mating pairs for the four species. To have a standard for comparing allometric patterns, allometry of aedeagal was compared to that of two non-genital traits, tibial, and fourth abdominal segment length. In all cases, the aedeagus was found to reach the rival sperm which supports the idea that stimulation is not the mechanism for sperm displacement but physical displacement. Aedeagal length was isometric, and its slope was lower in general compared to that of tibial length and fourth abdominal segment. Given that this isometric pattern is not common for other odonate species, our interpretation of these varying aedeagal scaling patterns in this insect order is that males’ and females’ sexual interests are in conflict (males are evolving an elongated aedeagus to reach rival sperm while females are evolving unreachable sperm storage organs to prevent displacement of stored sperm). This sexual conflict scenario would favor varying scaling patterns for aedeagal length in odonates. A final interpretation is that the risk of interspecific matings in damselflies, may also explain different species-specific, aedeagal allometries.

Ivermectin alters reproductive success, body condition and sexual trait expression in dung beetles

Ivermectin is a very common parasiticide used in livestock. It is excreted in the dung and has negative effects on survival and reproduction of dung-degrading organisms, including dung beetles. Here we exposed the dung beetle Euoniticellus intermedius to different concentrations of ivermectin in the food and evaluated reproductive success and the expression of traits associated with survival and reproduction under laboratory conditions. It is the first time the effects of ivermectin were evaluated on offspring physiological condition and the expression of a secondary sexual trait. We also registered the number of emerged beetles, sex ratio and body size of emerged adult beetles. Besides reducing the number of emerged beetles and body size, as found in the same and other insects, ivermectin at high doses reduced muscle mass while at intermediate doses it increased lipid mass. Ivermectin changed offspring sex ratio and at high doses increased the size of male horn, which is an important trait defining the male mating success. Our results highlight the importance of regulating parasiticide usage in livestock in order to maintain ecosystem services provided by dung beetles and confirm that contaminants impose new environmental conditions that not only impact on wild animal survival, but also on evolutionary processes such as sexual selection.

To be or not to be? Mating success and survival trade-offs when switching between alternative reproductive tactics.

Hormones underlie the decision of assuming a territorial or a nonterritorial role, with territorial individuals usually having higher hormonal levels than nonterritorial individuals. As a territorial status is linked to higher mating opportunities, it is unclear why animals do not keep high hormonal levels and one explanation is that this would imply survival costs. We have tested this using males of the territorial damselfly Argia emma in the field. We increased juvenile hormone (JH) levels using methoprene in both territorial and nonterritorial males and predicted that: (i) males will keep (the case of territorial males) or become (the case of nonterritorial males) territorial after hormonal increase, and (ii) there will be an increase in mating success for nonterritorial males only and an impaired survival for both male tactics. Hormonally treated males remained or became territorial but had their survival impaired compared with control groups. Also, hormonally treated, ex‐nonterritorial males increased their mating success compared with the other control, nonterritorial males. The reduced survival can be explained proximally by the energy devoted either to the enhanced aggression showed during territory defence or immune function (as detected previously in damselflies). Although nonterritorial males may increase their mating success by switching to a territorial tactic, they are possibly unable to do it naturally as JH is dietary dependent and usually nonterritorial animals are in poorer condition than territorial animals.