Me against who? Male guppies adjust mating behaviour according to their rival’s presence and attractiveness

This work was supported by Portuguese National Funds through FCT (Fundação para a Ciência e a Tecnologia), within the cE3c Unit FCT funding (grant number UID/BIA/00329/2013), IO PhD grant (SFRH/BD/90686/2012) and SAMV (SFRH/BPD/66042/2009 and PTDC/BIA‐ANM/0810/14) and MB (SFRH/BPD/82259/2011) Post‐Doctoral research grants. This work was also supported by the ERC (European Research Council) AdG BioTIME (250189) to AEM.Sexual selection theory suggests that males need to constantly reappraise their mating decisions to take account of the presence and the phenotypes of their rivals. Here we examine this expectation by asking: (i) If the presence of a rival influences male mating behaviour; (ii) How important is the attractiveness of the rival (absolute attractiveness) in shaping male behaviour; and (iii) How does a male's attractiveness in comparison to his rival (relative attractiveness) influence a male's mating decisions. Using the Trinidadian guppy, a species in which female mate choice (based on males’ attractive traits) plays an important role in male mating outcomes, we recorded the frequency of courtship displays and unsolicited attempts by focal males. First, we quantified focal male mating behaviour with and without a rival. Since the probability of a successful mating is, on average, halved by the presence of a rival, we predicted that under competition the focal male would invest more in less costly mating tactic—unsolicited attempts. Second, we examined how the rival's standard length and area of orange coloration mediated focal male mating behaviour. We found that rival presence influenced how focal males responded to females in terms of both mating tactics. However, the rival attractiveness elicited changes only in male courtship display. Focal males increased courtship display rate if his rival was small or if possessed large amounts of orange, regardless of considering rival absolute or relative attractiveness. Our results show that males invest in the costlier mating tactic when there is no rival or in the presence of a smaller rival. Interestingly, they make a similar investment in the presence of an attractive orange rival. Overall, this study highlights the importance of fine‐grained male decisions in mating encounters and shows that mating tactics are differentially shaped by multiple competition risk cues.PostprintPeer reviewe

Enemy within the gates : reasons for the invasive success of a guppy population (Poecilia reticulata) in Trinidad

The invasion of individuals into new habitats can pose a major threat to native species and to biodiversity itself. However, the consequences of invasions for native populations that are not fully reproductively isolated from their invaders are not yet well explored. Here I chose the Trinidadian guppy, Poecilia reticulata, to investigate how different population traits shaped the outcome of Haskins's introduction, a well-documented invasion of Guanapo river guppies into the Turure river. I especially concentrated on the importance of behaviour for invasive success. I investigated if the spread of Guanapo guppies is due to superiority in behaviour, life-history and/or genetics, or if the outcome of this translocation is due to chance. Despite the fact that by today the invasive front has passed the Turure's confluence with the River Quare many kilometres downstream of the introduction site, and the original genotype only survives in small percentages, as was revealed by genetic analysis in this and other studies, no obvious differences between invasive and native populations could be detected in any of the tested behavioural, life-history and genetic traits. When tested for mate choice, neither Guanapo nor Oropuche (Turure) males seemed to be able to distinguish between the population origin of females, but courted and mated at random. At the same time, females did not prefer to school with individuals of the same population over schooling with more distantly related females. The formation of mixed schools after an invasive event is therefore likely. Because female guppies showed a very low willingness to mate, even after having been separated from males for up to six months, sperm transfer through forced copulations will become more important. Taken together, these behaviours could increase the speed of population mixing after an invasion without the need for behavioural superiority of the invasive population. When tested for their schooling abilities, offspring of mixed parentage, in contrast to pure breds, displayed a large amount of variety in the time they spent schooling, a circumstance that can potentially influence survival rates and therefore the direction of gene pool mixing. Guanapo fish did not show reproductive superiority in a mesocosm experiment, where both populations were mixed in different proportions. On the contrary, in two out of three mixed treatments, the amount of Oropuche (Turure) alleles was significantly higher than expected from the proportion of initially stocked fish. The almost complete absence of distinguishable traits other than genetic variation between the examined populations that belong to different drainage systems, opposes the recent split of the guppy into two different species following drainage system borders, as is argued in this thesis. However, the successful invasion of the Turure by Guanapo guppies and the nearly entire disappearance of the original population can be explained in absence of differing population traits. Here I demonstrate how behavioural and genetic interactions between subspecies influence the outcome of biological invasions and second, how factors other than population traits, such as the geographic situation, can produce an advantageous situation for the invader even in the absence of population differences

Female brain size affects the assessment of male attractiveness during mate choice

Mate choice decisions are central in sexual selection theory aimed to understand how sexual traits evolve and their role in evolutionary diversification. We test the hypothesis that brain size and cognitive ability are important for accurate assessment of partner quality and that variation in brain size and cognitive ability underlies variation in mate choice. We compared sexual preference in guppy female lines selected for divergence in relative brain size, which we have previously shown to have substantial differences in cognitive ability. In a dichotomous choice test, large-brained and wild-type females showed strong preference for males with color traits that predict attractiveness in this species. In contrast, small-brained females showed no preference for males with these traits. In-depth analysis of optomotor response to color cues and gene expression of key opsins in the eye revealed that the observed differences were not due to differences in visual perception of color, indicating that differences in the ability to process indicators of attractiveness are responsible. We thus provide the first experimental support that individual variation in brain size affects mate choice decisions and conclude that differences in cognitive ability may be an important underlying mechanism behind variation in female mate choice

Ornamentos múltiples: Mecanismos, función y evolución.

[spa] El uso de señales múltiples de calidad es común en numerosas especies, pero este hecho no es fácil de explicar. Las presiones fluctuantes del ambiente podrían tener un rol importante en el origen y mantenimiento de las señales múltiples, y las implicaciones evolutivas de esta hipótesis enfatizan la importancia de realizar nuevos estudios sobre señales múltiples. En esta tesis se realizaron diferentes estudios sobre la señalización múltiple del plumaje de dos especies de aves: El carbonero común (Parus major) y el lúgano (Carduelis spinus). En el primer capítulo se examinó la banda alar amarilla del lúgano, un ornamento sexual basado en carotenoides. Se vio que machos con bandas alares mayores eran más rápidos resolviendo un problema de forrajeo. Esto sugiere la existencia de una selección sexual de habilidades cognitivas en el lúgano. En el segundo capítulo, estudiamos la función del babero negro del lúgano como señal de la personalidad del individuo. Descubrimos que lúganos con baberos de mayor tamaño mostraban tendencias exploratorias más rápidas. Este hallazgo apoya la idea de que los ornamentos del plumaje pueden funcionar como señales de la personalidad del individuo. En el tercer capítulo se examinó cómo las señales múltiples pueden definir el comportamiento sexual extra pareja. Se pudo constatar que la respuesta agonística y la paternidad de machos de carbonero dependía de la interacción entre la corbata negra y la coloración amarilla del pecho del macho, sugiriendo la existencia de diferentes estrategias reproductivas de acuerdo a la calidad individual. Por último, examinamos las posibles interacciones entre ornamentos sexuales y la familiaridad, mediante experimentos de selección de pareja en lúganos. Nuestros resultados sugieren que la familiaridad puede ser tan importante como los ornamentos sexuales a la hora de determinar los criterios de selección de la hembra. En conclusión, esta tesis profundiza en el hecho de que las diferentes cualidades de un individuo, reflejadas en distintas señales múltiples, tienen el potencial de ser parte de diferentes estrategias válidas en selección sexual y social, permitiendo una selección más plástica. Esta plasticidad de selección podría ser uno de los mecanismos tras el origen y mantenimiento de las señales múltiples.[eng] In sexual or social selection processes, animals employ traits that signal qualities. The use of multiple signals is known to be well spread in numerous species, but the ultimate reasons for using more than one single signal are not easy to explain. Why would animals invest in several different signals, instead of focusing on only one? Traditionally, the adaptive hypotheses formulated to explain the existence of multiple signalling have been framed into static scenarios, under constant selection pressures. However, there is increasing awareness of the need to widen this static framework, by taking into account the selection plasticity produced by spatial and temporal environmental heterogeneity. Fluctuating ecological and social environments could have an important role in the origin and maintenance of multiple signals. In an environment where changes happen faster every day, multiple signalling would allow a more flexible, dynamic selection, increasing the odds of survival and fitness. The evolutionary implications of this hypothesis highlight the importance of novel studies in multiple signalling. In this thesis, we performed several such experiments on the Eurasian siskin (Carduelis spinus) and the Great tit (Parus major). They are two passerine species that show ornaments based on melanins and carotenoids, which makes them a particularly suitable models for the study of multiple signalling. In the first chapter, the signalling function of the yellow wing stripe of the Eurasian siskin, a carotenoid based sexual ornament, was examined. A problem solving experiment showed that male siskins with longer yellow wing stripes were better foragers. These resuls suggest the existence of sexual selection for cognitive abilities. In the second chapter, we studied the function of the black bib of the Eurasian siskin as a potential source of information about the personality of the individual. We examined the exploratory behaviour of male siskins, finding that those with larger black bibs had a shorter approaching latency to a novel object. These results support the idea that plumage structures could give information about the personality of its bearer. The results of these two chapters show that colour signals based on different pigments have separate functions in the siskin, allowing multiple criteria in sexual (and social) selection. The third chapter examined the effects of different multiple colour signals on the extra pair sexual behaviour of the great tit. By measuring the response of different males to conspecific male intrusions, and the within pair paternity of males depending on their colour traits, we could observe that different combinations of traits where related to the intensity of nest defence, and implied differences in paternity loss. These findings suggest that males might be using different strategies to maximize their qualities. In the last chapter, we tested the potential interactions between colour sexual ornaments and the previous experience, by sexual selection experiments in siskins. Our results suggest that familiarity adds to attractiveness when female siskins choose a mate. At least in some species, females are using multiple criteria in mate choice, not necessarily related to external signals of quality. In conclusion, this thesis stress that multiple qualities, signalled by different colour traits, have the potential to be part of different successful social and sexual mate choice strategies, aiding a more plastic selection. Our results support the hypothesis that selection plasticity could be one of the mechanisms behind the origin and maintenance of multiple signal

Foraging, personality and parasites : investigations into the behavioural ecology of fishes

This thesis investigated differences in foraging behaviour, personality and parasitic infection, using behaviour experiments, traditional parasitology and molecular ecology. Five fish species, and a directly-transmitted ectoparasite, were used as model organisms. Evidence for a conservative foraging strategy was found in the four tropical fish species (Poecilia reticulata, P. sphenops, Xiphophorus maculates, X. hellerii) and in a temperate species (Gasterosteus aculeatus). In the latter, this behaviour was unaffected by social context, with no significant differences between isolated fish and shoals. Also, guppies showed a reduced acceptance of novel, conspicuously-coloured prey. Furthermore, using molecular scatology techniques, both prey and host species-specific DNA were detected in fish faecal samples so this methodology can be used in the future to examine diet in the wild. When considering the personality trait, boldness, guppies from two wild populations differed significantly in their relative boldness, but individuals within a single population were similar in their relative boldness. Boldness of fish was affected by mating, with virgin and pregnant females being bolder than their mated counterparts. Also, boldness impacted on shoaling behaviour, shy fish formed larger and tighter shoals than bold conspecifics. This had consequences for parasite transmission, with shy fish having higher parasite loads and a greater change in parasite load across an infection period than their bold counterparts. Furthermore, host contact was the main factor influencing transmission of a directly-transmitted ectoparasite within a group-living host species. Significantly more parasites were transmitted between hosts when hosts had more frequent and more prolonged contact with each other. Clearly, monitoring individual differences in various aspects of an animal's behaviour can answer many questions of ecological relevance, as well as discovering the evolutionary origins of such individual behavioural traits.EThOS - Electronic Theses Online ServiceGBUnited Kingdo

The role of conspecific social information on male mating decisions

Tese de doutoramento, Biologia (Etologia), Universidade de Lisboa, Faculdade de Ciências, 2018Behavioural plasticity occurs when animals adjust their behaviour to current environmental conditions. Research suggests that this ability helps animals cope with changeable environments, especially in the social domain, where social information is highly variable and unpredictable. In this thesis I evaluated the contribution of the complexity of social information to: 1) male mating behaviours, 2) evolution of courtship display, and 3) evolution of dishonest communication. For male mating behaviours, I performed experiments with guppies (Poecilia reticulata). I predicted that males would invest more on mating attempts if they spend more time without mating (chapter 2), and when there was a higher probability of mating success or fertilization success (chapters 3 and 4). I found that time between encounters with females (not time between actual mating opportunities) was determinant to male investment. Moreover, males did not avoid encountering competitors but invested more when they were the first to arrive near females (not the last), and when competing against more attractive males (but only for orange colouration). These evidences support that males produce complex plastic responses in face of diverse social information. For the evolution of courtship display and dishonest communication, my hypothesis was that competitor (bystander) males use the courtship performance of other males as information about their competitive ability, and that displayer males adjust their behaviour accordingly. For this, I performed systematic reviews (chapter 5), where I found that male male courtship display is, indeed, frequently associated with intrasexual competition, suggesting that courtship display has evolved a dual utility: attract females and intimidate competitors. A corollary of this, which I developed in a conceptual study (chapter 6), is that males can display dishonestly to deter competitors. If so, the interference of bystanders in communication systems could have a non-negligent role in the evolution of dishonest signalling

Playing Your Cards Right: How Guppies, Poecilia reticulata, Alter their Courtship Tactics in Varying Social Environments

This study examined how guppies, Poecilia reticulata, vary courtship behavior upon encountering social environments differing in sex ratio. I observed males and virgin females in social environments of varying sex ratios and noted the males’ display and sneaky copulation attempt frequencies, the time a male pursued the focal female, and female responsiveness. I also examined a focal pair’s courtship behavior over a 24-hr period and when in the presence of an audience male at different proximities to them. Males increased their display rates in a social environment with other individuals, significantly so in an all-male environment. Males also increased sneaky copulation attempt rates in the all-male and all-female environments. Females were more responsive to males with other individuals present than when alone with a focal male. Males did not adjust their courtship behavior in response to a single audience male, but they decreased their courtship behavior over 24-hrs. These results suggest guppies may adjust their courtship tactics in different social environments; in so doing they may maximize their mating success

Ontogenetic Environments and Female Mate Choice in Guppies, Poecilia Reticulata

Theoretical models of sexual selection assume that female mating preferences are fixed and variation found between individuals resulting solely from allelic variation at specific loci coding for sexual preferences. For the last decade, an increasing number of studies have demonstrated that individual phenotypic variation in preferences was common across a wide range of taxa and induced by the environmental context and the females’ condition. Further, developmental stages of life are crucial in the formation of behaviours in general and have proven to be determinant to learn sexual preferences in some species that dispense care for their young. However, very little studies have analysed how the early social and physical environments shape female mate choice in species that lack parental care. In this thesis, I used guppies (Poecilia reticulata), firstly, to investigate the influence of various aspects of the social environment provided by males during two ontogenetic phases. Secondly, I explored whether learned preferences in a foraging context during development could be transferred into a mating context. Considering the early social environment, I explored three distinctive features potentially displayed by males and that females might experience while growing. Females were reared with different values of a sexual trait not genetically preferred in the population (orange colour) and different values of a trait for which they had innate predisposition (total colour area). In both cases, females were exposed to the different treatments for the whole developmental period or for its later phase. My results indicated that females changed their sexual behaviours in response to both type of traits experienced, reversing sometimes their genetic preferences. Moreover, the timing of exposure seemed to be a key factor in the acquisition of preferences as females exposed only to the later part of development with different values of total colour didn’t rely anymore on colour patterns to discriminate among males. In a third body of experiment, I examined whether the overall phenotypic variance exhibited by males during whole development, independently of the values of a specific sexual cue, mediated female’s behaviours. In a context of high variance, female became choosier relatively to those experiencing less variance. As a response, males switched mating tactics and attempted more forced copulations. In its final part, my thesis searched for a link that might have arisen, owing to developmental conditions, between preferences using the same sensory modality in two behavioural contexts. Maturing females were given food that was associated to a certain colour and subsequently tested for both their coloured preference in a foraging and a sexual context. Although no foraging preference for the corresponding colour was detected, females that experienced a yellow stimulus preferred yellower males compared to females with other experiences. Taken together these results suggest that developmental conditions and especially the social environment play a pivotal role in the process of mate choice. Under some circumstances, learned mate preferences override genetically-based preferences highlighting the importance of non-genetic mechanisms. Accordingly, it is urgent to integrate in the study of sexual selection and reproductive isolation this dimension. In guppies, for instance, the effect of early social life might contribute to the maintenance of colour pattern polymorphism found in males

Foraging, personality and parasites: investigations into the behavioural ecology of fishes

This thesis investigated differences in foraging behaviour, personality and parasitic infection, using behaviour experiments, traditional parasitology and molecular ecology. Five fish species, and a directly-transmitted ectoparasite, were used as model organisms. Evidence for a conservative foraging strategy was found in the four tropical fish species (Poecilia reticulata, P. sphenops, Xiphophorus maculates, X. hellerii) and in a temperate species (Gasterosteus aculeatus). In the latter, this behaviour was unaffected by social context, with no significant differences between isolated fish and shoals. Also, guppies showed a reduced acceptance of novel, conspicuously-coloured prey. Furthermore, using molecular scatology techniques, both prey and host species-specific DNA were detected in fish faecal samples so this methodology can be used in the future to examine diet in the wild. When considering the personality trait, boldness, guppies from two wild populations differed significantly in their relative boldness, but individuals within a single population were similar in their relative boldness. Boldness of fish was affected by mating, with virgin and pregnant females being bolder than their mated counterparts. Also, boldness impacted on shoaling behaviour, shy fish formed larger and tighter shoals than bold conspecifics. This had consequences for parasite transmission, with shy fish having higher parasite loads and a greater change in parasite load across an infection period than their bold counterparts. Furthermore, host contact was the main factor influencing transmission of a directly-transmitted ectoparasite within a group-living host species. Significantly more parasites were transmitted between hosts when hosts had more frequent and more prolonged contact with each other. Clearly, monitoring individual differences in various aspects of an animal's behaviour can answer many questions of ecological relevance, as well as discovering the evolutionary origins of such individual behavioural traits

The Maintenance of Male Color Polymorphism in Poecilia parae

Genetic color polymorphisms are common in nature, and a major challenge for evolutionary biologists has been to understand how they are maintained despite the effects of directional selection. Recent studies suggest that frequency-dependent selection may explain the persistence of intraspecific variation in color. However, it remains to be determined whether frequency-dependent selection is the most predominant (or perhaps the only) mechanism to maintain such genetically-based polymorphisms. Using a South American fish, Poecilia parae, my dissertation aims to elucidate the relative roles of natural and sexual selection in the maintenance of polymorphisms in natural populations. Poecilia parae males exhibit five distinct, Y-linked and co-occurring color morphs: (i) `immaculata\u27, the smallest and drab-colored males that resemble juvenile females; (ii) `parae\u27, the largest males that exhibit a striped tail and black vertical body bars that intensify during social interactions; and (iii) the blue, red, and yellow morphs that are of intermediate body size and display colorful body flanks. Field surveys indicate that the frequency of each morph remains relatively stable and consistent over multiple years. Using a combination of observational and experimental studies, accompanied by techniques that aimed to characterize the visual ecology (e.g., water light transmission, visual sensitivity) of Poecilia parae, I found that this striking color polymorphism is maintained by a complex balance between different components of natural and sexual selection. First, males of the five color morphs employ different behavioral mating strategies (hereafter alternative mating strategies, AMSs) to maximize their reproductive success. These AMSs are also accompanied by differences in morphological traits, such as testes investment and sperm morphometry that complement the specific tactic. For instance, immaculata males are often categorized as an `unattractive\u27 male by females, which is correlated to its phenotypical appearance (smaller and drab). However, this morph is relatively abundant. I found that immaculata males specialize in `sneak\u27 copulations and have adaptations (i.e., larger testes and unique sperm morphology) that possibly confer a fertilization advantage during postcopulatory events, when competing with the sperm of more attractive males. My studies also indicate that females have strong mating preferences for red and yellow males, with visual predators also favoring those males as prey. These findings suggest that the antagonistic interaction between pre-mating sexual selection favoring and predation acting against the red and yellow morphs may prevent them from eliminating other color morphs from the population. In fact, the red and yellow males were consistently found to be the rarest morphs across populations. Further, despite overall preference for red or yellow males, my analysis also detected female preferences for blue males. These results suggest that the interaction between female mating preferences and predation accompanied by variation in male reproductive strategies may allow for the maintenance of complex color polymorphism in natural populations. Males of the different morphs further vary in their levels of aggressive behaviors. In a series of controlled lab experiments, I found that parae males gain successful matings by preventing other males from accessing females and/or modifying female mating preferences after test females witness successful agonistic interactions. Finally, I found that the signaling environment of Poecilia parae in nature is variable and that this contributes to temporal and spatial variation in how males are perceived by females. Although red males were typically the most conspicuous morph, blue males were sometimes more conspicuous than red males at several sampling sites. The results also revealed that an aquatic model predator is able to discriminate the same male color morphs that resulted also conspicuous for females. However, it is possible that males and females of Poecilia parae are using parts of the background spectral that are least sensitive for predators. In conclusion, my dissertation suggests that balancing selection defined by the interaction between various episodes of selection allows for the invasion of AMSs and thus the maintenance of the male color polymorphism in Poecilia parae