Miguel Barbosa

Fitness consequences of female multiple mating: A direct test of indirect benefits

BackgroundThe observation that females mate multiply when males provide nothing but sperm - which sexual selection theory suggests is unlikely to be limiting - continues to puzzle evolutionary biologists. Here we test the hypothesis that multiple mating is prevalent under such circumstances because it enhances female fitness. We do this by allowing female Trinidadian guppies to mate with either a single male or with multiple males, and then tracking the consequences of these matings across two generations.ResultsOverall, multiply mated females produced 67% more F2 grand-offspring than singly mated females. These offspring, however, did not grow or mature faster, nor were they larger at birth, than F2 grand-offspring of singly mated females. Our results, however, show that multiple mating yields benefits to females in the form of an increase in the production of F1. The higher fecundity among multiply mated mothers was driven by greater production of sons but not daughters. However, contrary to expectation, individually, the offspring of multiply mated females do not grow at different rates than offspring of singly mated females, nor do any indirect fitness benefits or costs accrue to second-generation offspring.ConclusionsThe study provides strong evidence that multiple mating is advantageous to females, even when males contribute only sperm. This benefit is achieved through an increase in fecundity in the first generation, rather than through other fitness correlates such as size at birth, growth rate, time to sexual maturation and survival. Considered alongside previous work that female guppies can choose to mate with multiple partners, our results provide compelling evidence that direct fitness benefits underpin these mating decisions.

Ontogenetic shifts in patterns of microhabitat utilization in the small-headed clingfish, Apletodon dentatus (Gobiesocidae)

The patterns of microhabitat utilization by the clingfish Apletodon dentatus were investigated, based on SCUBA diving surveys at the Arrábida Marine Park (Portugal). In all inspected microhabitats, this species was only found in algal turfs, sea urchins and boulders. The association of A. dentatus with sea urchins is here analysed for the first time. There was a differential utilization of the microhabitats, with small juveniles recruiting to algal turfs, intermediate individuals found in association with the sea urchins Paracentrotus lividus and Sphaerechinus granularis and larger fish occurring mainly in boulders. The depth distribution patterns are also analysed.

Effects of polyandry on male phenotypic diversity

Polyandry has the potential to affect the distribution of phenotypes and to shape the direction of sexual selection. Here, we explore this potential using Trinidadian guppies as a model system and ask whether polyandry leads to directional and/or diversifying selection of male phenotypic traits. In this study, we compare the phenotypic diversity of offspring from multiply and singly sired broods. To quantify phenotypic diversity, we first combine phenotypic traits using multivariate methods, and then take the dispersion of individuals in multivariate space as our measure of diversity. We show that, when each trait is examined separately, polyandry generates offspring with a higher proportion of bright coloration, indicating directional selection. However, our multivariate approach reveals that this directionality is accompanied by an increase in phenotypic diversity. These results suggest that polyandry (i) selects for the production of sons with the preferred brighter colour phenotypes whereas (ii) enhancing the diversity of male sexual traits. Promoting phenotypic diversity may be advantageous in coping with environmental and reproductive variability by increasing long‐term fitness.

Evidence of female-promoted polyandry in Trinidadian guppies

Polyandry is extremely common across a wide range of organisms. In promiscuous mating systems, females are often sexually harassed by males, but at the same time obtain benefits from multiple mating. It remains unclear whether polyandry is exclusively imposed by males or is also promoted by females. Here, we investigated this question by recording the time spent by female guppies near a single male or a group of males with similar size and colour patterns over three consecutive days. We accounted for the effect of shoaling by using a control treatment where a group of females was used instead of a group of males. Results showed that females spent significantly more time near the group of males, but not with the group of females. In the presence of a group of males, total female mating preference time did not change over the course of the study, but rather shifted from spending more time near the single male at the beginning of the experiment to spending more time near the group of males. The consequence of this female preference for associating with a group of males in a non-experimental setup would be to promote multiple mating. Our result indicates that polyandry in guppies is at least partially encouraged by females, and not entirely a consequence of male sexual behaviour.

Predation life history responses to increased temperature variability

The evolution of life history traits is regulated by energy expenditure, which is, in turn, governed by temperature. The forecasted increase in temperature variability is expected to impose greater stress to organisms, in turn influencing the balance of energy expenditure and consequently life history responses. Here we examine how increased temperature variability affects life history responses to predation. Individuals reared under constant temperatures responded to different levels of predation risk as appropriate: namely, by producing greater number of neonates of smaller sizes and reducing the time to first brood. In contrast, we detected no response to predation regime when temperature was more variable. In addition, population growth rate was slowest among individuals reared under variable temperatures. Increased temperature variability also affected the development of inducible defenses. The combined effects of failing to respond to predation risk, slower growth rate and the miss-match development of morphological defenses supports suggestions that increased variability in temperature poses a greater risk for species adaptation than that posed by a mean shift in temperature.

Maternal response to environmental unpredictability

Abstract Mothers are expected to use environmental cues to modify maternal investment to optimize their fitness. However, when the environment varies unpredictably, cues may not be an accurate proxy of future conditions. Under such circumstances, selection favors a diversifying maternal investment strategy. While there is evidence that the environment is becoming more uncertain, the extent to which mothers are able to respond to this unpredictability is generally unknown. In this study, we test the hypothesis that Daphnia magna increase the variance in maternal investment in response to unpredictable variation in temperature consistent with global change predictions. We detected significant variability across temperature treatments in brood size, neonate size at birth, and time between broods. The estimated variability within‐brood size was higher (albeit not statistically significant) in mothers reared in unpredictable temperature conditions. We also detected a cross‐generational effect with the temperature history of mothers modulating the phenotypic response of F1s. Notably, our results diverged from the prediction that increased variability poses a greater risk to organisms than changes in mean temperature. Increased unpredictability in temperature had negligible effects on fitness‐correlated traits. Mothers in the unpredictable treatment, survived as long, and produced as many F1s during lifetime as those produced in the most fecund treatment. Further, increased unpredictability in temperature did not affect the probability of survival of F1s. Collectively, we provide evidence that daphnia respond effectively to thermal unpredictability. But rather than increasing the variance in maternal investment, daphnia respond to uncertainty by being a jack of all temperatures, master of none. Importantly, our study highlights the essential need to examine changes in variances rather than merely on means, when investigating maternal responses.

How pre- and postcopulatory sexual selection influence male mating decisions in a promiscuous species

When females mate multiply, male reproductive success depends on both pre- and postcopulatory processes, including female choice and sperm competition. However, these processes can favour different mating tactics in males. Here we used the Trinidadian guppy, Poecilia reticulata, system to understand how this conflict is resolved. We asked whether knowledge of recent female mating history leads males to adjust their mating effort with respect to the time devoted to mating activity, and the frequency and the sequence of mating tactics employed. To do this we quantified male mating behaviour in three competitive scenarios: (1) Single, when a focal male arrives near a single female and remains alone with her; (2) First, when a focal male is joined by a rival male; and (3) Second, when a focal male arrives after a rival male. We hypothesized that males adjust their behaviour based on arrival order. If female sequential mate choice is the main process shaping male mating behaviours (favouring First males in guppies), males should avoid competition and invest most when Single. Alternatively, if last-male sperm precedence is the major driver of decision making, males should invest more in mating attempts in the Second scenario. Greatest investment when First implies an intermediate strategy. We found that order of arrival influenced mating decisions with most mating activity during the First rather than the Single and Second scenarios. This result suggests that both pre- and postcopulatory processes influence mating investment, and that individual males make contingent decisions to maximize both mating and fertilization success.

Synergy effects of fluoxetine and variability in temperature lead to proportionally greater fitness costs in Daphnia: A multigenerational test

Increased variability in water temperature is predicted to impose disproportionally greater fitness costs than mean increase in temperature. Additionally, water contaminants are currently a major source of human-induced stress likely to produce fitness costs. Global change models forecast an increase in these two human-induced stressors. Yet, in spite the growing interest in understanding how organisms respond to global change, the joint fitness effects of water pollution and increased variability in temperature remain unclear. Here, using a multigenerational design, we test the hypothesis that exposure to high concentrations of fluoxetine, a human medicine commonly found in freshwater systems, causes increased lifetime fitness costs, when associated with increased variability in temperature. Although fluoxetine and variability in temperature elicited some fitness cost when tested alone, when both stressors acted together the costs were disproportionally greater. The combined effect of fluoxetine and variability in temperature led to a reduction of 37% in lifetime reproductive success and a 17.9% decrease in population growth rate. Interestingly, fluoxetine and variability in temperature had no effect on the probability of survival. Freshwater systems are among the most imperilled ecosystems, often exposed to multiple human-induced stressors. Our results indicate that organisms face greater fitness risk when exposed to multiple stressors at the same time than when each stress acts alone. Our study highlights the importance of using a multi-generational approach to fully understand individual environmental tolerance and its responses to a global change scenario in aquatic systems.

Forced monogamy in a multiply mating species does not impede colonisation success.

BackgroundThe guppy (Poecilia reticulata) is a successful invasive species. It is also a species that mates multiply; previous studies have demonstrated that this strategy carries fitness benefits. Guppies are routinely introduced to tanks and troughs in regions outside their native range for mosquito-control purposes, and often spread beyond these initial confines into natural water bodies with negative ecological consequences. Here, using a mesocosm set up that resembles the containers into which single guppies are typically introduced for mosquito control, we ask whether singly-mated females are at a disadvantage, relative to multiply-mated females, when it comes to founding a population. Treatments were monitored for one year.ResultsA key finding was that mating history did not predict establishment success, which was 88% in both treatments. Furthermore, analysis of behavioural traits revealed that the descendants of singly-mated females retained antipredator behaviours, and that adult males showed no decrease in courtship vigour. Also, we detected no differences in behavioural variability between treatments.ConclusionsThese results suggest that even when denied the option of multiple mating, singly-mated female guppies can produce viable populations, at least at the founder stage. This may prove to be a critical advantage in typical introduction scenarios where few individuals are released into enclosed water bodies before finding their way into natural ecosystems.

Individual variation in reproductive behaviour is linked to temporal heterogeneity in predation risk

Variation in predation risk is a major driver of ecological and evolutionary change, and, in turn, of geographical variation in behaviour. While predation risk is rarely constant in natural populations, the extent to which variation in predation risk shapes individual behaviour in wild populations remains unclear. Here, we investigated individual differences in reproductive behaviour in 16 Trinidadian guppy populations and related it to the observed variation in predator biomass each population experienced. Our results show that high heterogeneity in predator biomass is linked to individual behavioural diversification. Increased within-population heterogeneity in predator biomass is also associated with behavioural polymorphism. Some individuals adjust the frequency of consensual mating behaviour in response to differences in sex ratio context, while others display constantly at elevated frequencies. This pattern is analogous to a ‘live fast, die young’ pace-of-life syndrome. Notably, both high and low mean differences in predator biomass led to a homogenization of individual frequency of consensual mating displays. Overall, our results demonstrate that individual behavioural variation is associated with heterogeneity in predator biomass, but not necessarily with changes in mean values of predator biomass. We suggest that heterogeneity in predator biomass is an informative predictor of adaptive responses to changes in biotic conditions.