Terminal Reproductive Investment Research Articles

Environmental correlates of circannual breeding periodicity in a multi-species assemblage of Amazonian electric fishes

We quantified patterns of circannual reproductive breeding periodicity in a multi-species assemblage of the gymnotiform knifefish genus Brachyhypopomus from Amazonian floodplain and terra firme stream habitats. We applied linear mixed-effect models and model selection to a dataset of 3205 fish from the five most abundant species to identify environmental variables predictive of gonadosomatic index (GSI) – including rainfall, river level, water temperature, conductivity, dissolved oxygen (DO), and pH. A single common floodplain species exhibited a well-demarcated ca. 6-month breeding season corresponding to the rising-water and high-water period. In this species the strongest predictors of GSI in both sexes were river level and pH. Conductivity, temperature, and DO all exhibited substantial circannual variation in the floodplain but were uncorrelated to GSI. Four common terra firme stream-dwelling species exhibited longer (ca. 7–9-month) and less distinct breeding seasons that were approximately coincident with the late dry/early rainy season. The stream species exhibited a congruent species-wide response in which GSI was predicted in both sexes by rainfall, but not by physico-chemical water properties (all of which exhibited relatively minor circannual variation). Five of the most abundant species in this study have a semelparous one-year life history, but one (B. beebei) has an iteroparous two-year life history. Consistent with a pattern of terminal reproductive investment, we observed a more pronounced elevation of GSI (especially in females) in B. beebei’s final second breeding season than in its first.

Immunity for nothing and the eggs for free: Apparent lack of both physiological trade-offs and terminal reproductive investment in female crickets (Gryllus texensis).

Should females alter their reproductive strategy when attacked by pathogens? Two hypotheses provide opposite predictions. Terminal reproductive investment theory predicts that reproduction should increase when the risk of death increases. However, physiological trade-offs between reproduction and immune function might be expected to produce a decrease in reproduction during a robust immune response. There is evidence for both hypotheses. We examine whether age determines the effect of an immune challenge on reproductive strategy in long-winged females of the Texas field cricket, Gryllus texensis, when fed an ecologically valid (i.e. limited) diet. The limited diet reduced reproductive output. However, even under resource-limited conditions, immune challenge had no effect on the reproductive output of young or middle-aged females. Both reproductive output and immune function (lysozyme-like activity and phenoloxidase (PO) activity) increased with age, which is contrary to both hypotheses. We hypothesize that PO activity is pleiotropic and represents an investment in both reproduction and immune function. Three proPO genes (identified in a published RNA-seq dataset (transcriptome)) were expressed either in the fat body or the ovaries (supporting the hypothesis that PO is bifunctional). The possible bifunctionality of PO suggests that it may not be an appropriate immune measure for studies on immune/reproductive trade-offs. This study also suggests that the threshold for terminal reproductive investment may not decrease prior to senescence in some species.

Differential effects of predator cues versus activation of fight-or-flight behaviour on reproduction in the cricket Gryllus texensis

How prey animals determine predation risk remains uncertain. We propose that one signal of high predation risk is repeated activation of fight-or-flight behaviour. We activated escape runs in the cricket Gryllus texensis by blowing air on the cerci. Escape runs were induced for 5 min, three times per day, three times per week for 4 weeks. Repeated fight-or-flight behaviour led to a loss in mass and decreased life span, suggesting a decline in somatic maintenance. However, there was an increase in egg laying, which we interpret as terminal reproductive investment. Stress responses remained robust. Octopamine (OA), a stress neurohormone in insects, increased in concentration in the haemolymph after running, and the magnitude of the increase was the same even after repeated activation (i.e. there was no habituation of the response). There was also no increase in basal OA haemolymph levels. In a second experiment, crickets were exposed to a mantid (predator, Tenodera sinensis), a walking stick (nonpredator, Carausius morosus), or an empty container. None of the crickets exhibited fight-or-flight behaviour. However, mantid-exposed crickets decreased egg laying. There was no decrease in life span or mass. There was no change in basal levels of OA, or in the magnitude of the OA increase after running. These results are consistent with the hypothesis that repeated fight-or-flight behaviour induces reproductive responses that would be adaptive for a shortened life span. These responses differ from those produced by predator cues alone. Even short-lived animals, such as crickets, appear to alter reproduction depending on the relative predation risk and their residual reproductive potential.

Effect of immune challenge on aggressive behaviour: how to fight two battles at once

Animals are attacked by pathogens, predators and competitors, sometimes simultaneously. For example, male crickets fight each other for access to females and such challenges may occur when one or both males are also defending themselves against a pathogen. We tested whether males altered their aggressive motivation when faced with both a competitor and a pathogen simultaneously. We found that immune-challenged male crickets (Gryllus texensis) were more likely to defeat male competitors when the reproductive payoff (i.e. a female) was nearby. However, when females were not present, males showed a decrease in their aggressive behaviour, and were less likely to win encounters with control males. This plasticity of aggressive motivation did not occur when males were chronically immune challenged. Chronically immune-challenged males were more likely to be defeated by control males regardless of the presence of a female. These results suggest that the costs associated with a chronic immune challenge may prevent terminal reproductive investment. We show that males can benefit from terminal reproductive investment because acutely immune-challenged males were still capable of mating and females did not appear to discriminate against them. Male crickets appear to engage in a context-dependent trade-off between the ability to defeat pathogens and the ability to defeat competitors. This trade-off is mediated, in part, by changes in male aggressive motivation (i.e. the critical threshold for the decision to flee).

Immune activation generates corticosterone-mediated terminal reproductive investment in a wild bird.

Despite classical expectations of a trade-off between immune activity and reproduction, an emergent view suggests that individuals experiencing activation of their immune system actually increase reproductive effort and allocation to offspring as a form of terminal investment in response to reduced survival probability. However, the components and mechanisms of increased parental investment following immunostimulation are currently unknown. We hypothesize that increased glucocorticoid production following immunostimulation modulates the increase in reproductive effort that constitutes terminal investment. We activated the immune system of breeding female house wrens (Troglodytes aedon) with an immunogen and cross-fostered the eggs that they subsequently produced to separate prenatal and postnatal components of maternal investment. Cross-fostering revealed an increase in both pre- and postnatal allocation from immunostimulated females, which was confirmed by quantification of egg constituents and maternal provisioning behavior. The increase in maternal provisioning was mediated, at least in part, by increased corticosterone in these females. Offspring immune responsiveness was also enhanced through transgenerational immune priming via the egg. Thus, our results indicate that maternal immunostimulation induces transgenerational effects on offspring through both pre- and postnatal parental effects and support an important role for corticosterone in mediating parental investment.

Parasitic aphrodisiacs: manipulation of the hosts' behavioral defenses by sexually transmitted parasites.

Animals have a number of behavioral defenses against infection. For example, they typically avoid sick conspecifics, especially during mating. Most animals also alter their behavior after infection and thereby promote recovery (i.e., sickness behavior). For example, sick animals typically reduce the performance of energetically demanding behaviors, such as sexual behavior. Finally, some animals can increase their reproductive output when they face a life-threatening immune challenge (i.e., terminal reproductive investment). All of these behavioral responses probably rely on immune/neural communication signals for their initiation. Unfortunately, this communication channel is prone to manipulation by parasites. In the case of sexually transmitted infections (STIs), these parasites/pathogens must subvert some of these behavioral defenses for successful transmission. There is evidence that STIs suppress systemic signals of immune activation (e.g., pro-inflammatory cytokines). This manipulation is probably important for the suppression of sickness behavior and other behavioral defenses, as well as for the prevention of attack by the host's immune system. For example, the cricket, Gryllus texensis, is infected with an STI, the iridovirus IIV-6/CrIV. The virus attacks the immune system, which suffers a dramatic decline in its ability to make proteins important for immune function. This attack also hampers the ability of the immune system to activate sickness behavior. Infected crickets cannot express sickness behavior, even when challenged with heat-killed bacteria. Understanding how STIs suppress sickness behavior in humans and other animals will significantly advance the field of psychoneuroimmunology and could also provide practical benefits.

Evolution: Exposing the Buried Costs of Reproduction

Investigating the cost of reproduction and terminal reproductive investment is difficult in most species as individuals can respond plastically to most brood manipulations. Experiments in a burying beetle provide new insight into the allocation of resources towards current and future reproductive events.

Wounding‐mediated gene expression and accelerated viviparous reproduction of the pea aphid Acyrthosiphon pisum

Most insects mount a potent antimicrobial defence upon contact with microbes or microbe-associated pattern molecules. Using a combined set of methods for analysis of insect innate immunity, we report here that piercing of the pea aphid Acyrthosiphon pisum with a bacteria-contaminated needle elicits lysozyme-like activity in the haemolymph but no detectable activities against live bacteria. Confirming these results, we found no homologues of known antimicrobial peptides in our cDNA library generated by using the suppression subtractive hybridization method or in over 90,000 public expressed sequence tag (EST) sequences, but lysozyme genes have recently been described in A. pisum. Interestingly, we discovered that production of viviparous offspring was significantly accelerated upon wounding. Therefore, we postulate that aphids may increase terminal reproductive investment and limit antibacterial defence in response to a threat to their survival.

Why twin pregnancies are more successful at advanced than young maternal age? A potential role of 'terminal reproductive investment'

Why twin pregnancies are more successful at advanced than young maternal age? A potential role of 'terminal reproductive investment'

Why Are Males Bad for Females? Models for the Evolution of Damaging Male Mating Behavior

One explanation for the cost to mating for females caused by damaging male mating behavior is that this causes the females to adaptively modify their subsequent life histories in a way that also increases male fitness. This might occur because the reduction in residual reproductive value of the female increases her optimal oviposition rate or because an increase in the current level of damage increases the female's optimal remating interval. In this article, I present models of a stochastic dynamic game in which males choose the level of mating damage that they inflict on females and females choose their oviposition rate and whether to remate. The models show that some level of damage is always an evolutionarily stable strategy and may even provoke females into making terminal reproductive investment (and hence a semelparous life history), that nondamaging populations are always invaded by damaging male mutants, and that damage evolves because of its effect on oviposition rate and despite its effect on remating interval.

Spontaneous male death during copulation in an orb-weaving spider

Males of some cannibalistic species of spiders and insects appear to sacrifice themselves by allowing the female to eat them, and the adaptive significance of such drastic terminal reproductive investment has recently been demonstrated for a spider. Typically, the female has to kill the male, but it has been suggested that males of some species in the cannibalistic orb-weaving spider genus Argiope may die in copula without female 'collaboration'. Here, we provide the first experimental evidence to our knowledge of programmed sudden death after onset of copulation in males of the spider Argiope aurantia. Our observations reveal that males invariably die during the insertion of their second pedipalp, regardless of whether they mate with newly moulted, defenceless females or with older mature females that often attack them. We determined experimentally that the death of males is triggered immediately upon insertion of the second palp, when males become unresponsive, and heartbeat ceases within minutes of insertion. We discuss the possible adaptive significance of programmed death during copulation, and argue that male death has evolved in a context other than sexual cannibalism.