Simona Kralj-Fišer

Studying personality variation in invertebrates: why bother?

Research on animal personality variation has been burgeoning in the last 20 years but surprisingly few studies have investigated personalities in invertebrate species although they make up 98% of all animal species. Such lack of invertebrate studies might be due to a traditional belief that invertebrates are just ‘minirobots’. Lately, studies highlighting personality differences in a range of invertebrate species have challenged this idea. However, the number of invertebrate species investigated still contrasts markedly with the effort that has been made studying vertebrates, which represent only a single subphylum. We describe how investigating proximate, evolutionary and ecological correlates of personality variation in invertebrates may broaden our understanding of personality variation in general. In our opinion, personality studies on invertebrates are much needed, because invertebrates exhibit a range of aspects in their life histories, social and sexual behaviours that are extremely rare or absent in most studied vertebrates, but that offer new avenues for personality research. Examples are complete metamorphosis, male emasculation during copulation, asexual reproduction, eusociality and parasitism. Further invertebrate personality studies could enable a comparative approach to unravel how past selective forces have driven the evolution of personality differences. Finally, we point out the advantages of studying personality variation in many invertebrate species, such as easier access to relevant data on proximate and ultimate factors, arising from easy maintenance, fast life cycles and short generation times.

Individual behavioural consistency and plasticity in an urban spider

Behaviour is generally plastic to some degree and allows an animal to react appropriately to changing and novel conditions. Consequently, a degree of plasticity is predicted to be a key determinant of an organism’s ability to cope with novel (e.g. urban) environments. Yet behavioural plasticity is often genetically determined and many animals exhibit personalities (i.e. consistent between-individual differences in behaviours). We explored the degree of behavioural plasticity versus personality in the bridge spider, Larinioides sclopetarius, which occurs in extremely high densities in urban areas over the Holarctic. The spiders show extraordinary plasticity in life history. We investigated between- and withinindividual variability, correlations and heritability for aggressiveness, boldness, behaviours in novel environment, and voracity towards prey. We predicted that these spiders would show high individual behavioural plasticity or that there would be a mix of individuals with different personalities. We found temporal consistency and moderate heritability in intra-sex aggressiveness and boldness, whereas behaviours in novel environment were repeatable but not heritable. Most behavioural traits showed high between-individual variability. We discuss the idea that low heritability of behaviours related to foraging success and a lack of behavioural correlations may be a result of developmental plasticity as a mechanism that promotes success in cities. In the next step, we experimentally tested whether composition of aggressiveness types affects spiders’ mass gain and survival in a high-density group. Groups of only aggressive types had highest mass but also showed highest mortality, although not significantly. Our results lend support to the hypothesis that living in high densities does not necessarily require a reduction of mean aggressiveness levels but that a polymorphism in aggressive personalities main

Individual- and condition-dependent effects on habitat choice and choosiness

Research on consistent individual differences in behavior, or “behavioral syndromes”, continues to grow rapidly, and yet, the aspects of behavior under consideration have remained remarkably limited. Here, we consider individual variation in consistency of choice (termed here “choosiness”), as expressed during habitat choice. We repeatedly tested the responses of female Western Black Widows, Latrodectus hesperus, to two cues of habitat quality: prey chemical cues and variation in web site illuminance. We estimated females’ response by the distance they positioned themselves from (1) the source of prey chemical cues and (2) the darkest edge of our test arena. Individuals with low variance in their responses are deemed more “choosy”, whereas individuals with high variance are deemed less “choosy”. Generally, most females initiated web construction near the source of the prey chemical cues and tended to place themselves in low-light conditions. However, we detected strong, repeatable differences in females’ intensity of response, and within-individual variance of response (i.e., choosiness) was correlated across situations: females with highly consistent responses towards cricket chemical cues also exhibited highly consistent responses towards variation in light conditions. When deprived of food for extended periods, females were indistinguishable in their responses towards prey chemical cues, but tended to initiate web construction in brighter lighting conditions. Food-deprived females universally exhibited higher variance and diminished consistency in their responses (i.e., they were less choosy). Additionally, higher choosiness was associated with greater mass loss during choice trials, suggesting choosiness is energetically costly. Our results demonstrate that consistency of response to environmental cues is yet another element of behavior that varies among individuals and variation in choosiness could beget speed/quality trade-offs during animal decision making.

Behavioural and physiological correlates of personality in greylag geese (Anser anser)

Personality means suites of correlated behavioural traits, also referred to as “behavioural syndromes” or “personality dimensions”. Across animal taxa similar combinations of traits seem to prevail, which may have proximate foundation in common neuroendocrine mechanisms. Hitherto, these have been rarely studied in intact social settings. We investigated personalities of greylag goose males from a free-roaming flock that shows complex social relationships. In connection with our longitudinal study on the consistency of behavioural and physiological responses to multiple challenges, we asked whether and how single, personality-related behavioural traits correlate with each other to form personality dimension(s). We tested whether these dimensions were related to physiological characteristics that previously showed limited plasticity (heart rate (HR), baseline and stress-induced excreted immuno-reactive corticosterone (BM), and testosterone metabolites levels) and, furthermore, to age, body measures, and dominance rank. Principal-components analysis based on behavioural variables revealed two factors: 51.1% of variability was explained by “aggressiveness” and a further 19.1% by “sociability”. “Aggressiveness” comprised correlated measures of aggression, subordinance, boldness, vigilance, and proximity to the mate. This “aggressiveness” positively correlated with stress-induced BM levels, the HR increase during aggressive interactions, and with dominance rank, which may suggest proximate and functional contingencies of this personality dimension.

Mate quality, not aggressive spillover, explains sexual cannibalism in a size dimorphic spider

Sexual cannibalism particularly before mating is costly for the male victim but also for the female aggressor if she risks remaining unmated. The aggressive spillover hypothesis explains the persistence of this behavior as a maladaptive side effect of positive selection on aggressiveness in a foraging context. The hypothesis predicts that the occurrence of sexual cannibalism is explained by female aggressiveness but is not related to male phenotype or behavioral type. An alternative hypothesis invokes sexual selection and makes the opposite prediction namely that sexual cannibalism is an expression of female choice and should hence mainly target males of low quality. We tested the above hypotheses on a sexually dimorphic nephilid spider Nephilengys livida, known for male monopolization of females via genital damage, female genital plugging, and mate guarding, by staging mating trials during which we recorded mating behaviors and occurrences of pre- and postcopulatory cannibalism. We did not restrict assessment of aggressiveness to the mating and foraging context but also included aggression against same sex conspecifics. To assess female personalities, i.e., consistent individual differences in behavior including aggressiveness, we repeatedly tested them for intra-sex aggression, voracity towards prey, locomotory activity, and boldness. Females exhibited consistent differences in intra-sex aggressiveness, latency to attack prey, and boldness. Aggressive females had shorter latencies to attack prey and were more active than non-aggressive ones. In contrast to the predictions of the aggressive spillover hypothesis, females that were aggressive towards prey and towards other females were not more likely to attack a male than non-aggressive females. In support of the mate choice hypothesis, less aggressive males were more likely attacked and cannibalized than more aggressive ones. This hints at sexual selection for aggressiveness in males and raises the question of mechanisms that maintain variation in male aggressiveness.

Eunuchs are better fighters

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.

Remote copulation: male adaptation to female cannibalism.

Sexual cannibalism by females and associated male behaviours may be driven by sexual conflict. One such male behaviour is the eunuch phenomenon in spiders, caused by total genital emasculation, which is a seemingly maladaptive behaviour. Here, we provide the first empirical testing of an adaptive hypothesis to explain this behaviour, the remote copulation, in a highly sexually cannibalistic orb-web spider Nephilengys malabarensis. We demonstrate that sperm transfer continues from the severed male organ into female genitals after the male has been detached from copula. Remote copulation increases the total amount of sperm transferred, and thus probably enhances paternity. We conclude that the mechanism may have evolved in response to sexual cannibalism and female-controlled short copulation duration.

Mating Plugs in Polyandrous Giants: Which Sex Produces Them, When, How and Why?

Background Males usually produce mating plugs to reduce sperm competition. However, females can conceivably also produce mating plugs in order to prevent unwanted, superfluous and energetically costly matings. In spiders–appropriate models for testing plugging biology hypotheses–mating plugs may consist of male genital parts and/or of amorphous covers consisting of glandular or sperm secretions. In the giant wood spider Nephila pilipes, a highly sexually dimorphic and polygamous species, males are known to produce ineffective embolic plugs through genital damage, but nothing is known about the origin and function of additional conspicuous amorphous plugs (AP) covering female genitals. Methodology We tested alternative hypotheses of the nature and function of AP in N. pilipes by staging mating trials with varying degrees of polyandry. No APs were ever formed during mating trials, which rules out the possibility of male AP formation. Instead, those females that oviposited produced the AP from a liquid secreted during egg sac formation. Polyandrous females were more likely to lay eggs and to produce the AP, as were those that mated longer and with more total insertions. Our further tests revealed that, in spite of being a side product of egg sac production, AP, when hardened, prevented any subsequent copulation. Conclusions We conclude that in the giant wood spider (Nephila pilipes), the amorphous mating plugs are not produced by the males, that repeated copulations (most likely polyandrous) are necessary for egg fertilization and AP formation, and that the AP represents a female adaptation to sexual conflict through prevention of unwanted, excessive copulations. Considering the largely unknown origin of amorphous plugs in spiders, we predict that a similar pattern might be detected in other clades, which would help elucidate the evolutionary interplay of various selection pressures responsible for the origin and maintenance of mating plugs.

Eunuchs as better fighters

Male–male competition for females can significantly affect a male’s reproductive success and hence his fitness. Game theory predicts that an individual should avoid fighting when its future reproductive potential is high, but should fight forcefully when its future reproductive potential is insignificant. When mates are scarce, extreme competition and fatal fighting is expected. We recently showed that Nephilengys malabarensis eunuchs, i.e. sterile spider males that lost their genitals during copulation, become more aggressive during male–male contests. Here, we add crucial comparative data by exploring eunuch fighting behaviour in Nephilengys livida from Madagascar, specifically by testing the ‘better fighter hypotheses’ in a laboratory setting. Similar to N. malabarensis, N. livida copulations resulted in total male castration with the severed palp plugging the female genitals in 70.83% cases, which mostly (63.63%) prevented subsequent copulations. Unexpectedly, however, N. livida eunuchs exhibited lower aggressiveness than virgin males. We interpret these results in the light of different mating biology between the so far studied species known for the eunuch phenomenon, which might reflect differing plug effectiveness due to variation in genital anatomy in N. livida, N. malabarensis and Herennia multipuncta. However, detected differences in aggressive behaviour of N. livida versus N. malabarensis eunuchs might also be explained by the species’ ecology, with lower population densities resulting in a relaxed male–male competition making excessive aggression and mate guarding redundant. This study thus questions the generality of overt aggressiveness in mated males with no reproductive value, and highlights the importance of understanding the natural history of species in the question.

Emasculation: gloves-off strategy enhances eunuch spider endurance

Males of sexually cannibalistic spiders commonly mutilate parts of their paired genitals (palps) during copulation, which may result in complete emasculation or the ‘eunuch phenomenon’. In an orb-web nephilid spider, Nephilengys malabarensis, about 75 per cent of males fall victim to sexual cannibalism, and the surviving males become half-eunuchs (one palp emasculated) or full-eunuchs (both palps emasculated). While it has been shown that surviving eunuchs are better fighters compared with intact males when guarding the females with which they have mated, mechanisms behind eunuchs’ superior fighting abilities are unknown. The previously proposed ‘gloves-off’ hypothesis, attributing eunuchs’ enhanced locomotor endurance to the reduction in total body weight caused by genital mutilation, is plausible but has remained untested. Here, we tested the gloves-off hypothesis in N. malabarensis by comparing the time until exhaustion (i.e. endurance) of intact males with half- and full-eunuchs created experimentally. We found that by reducing body weight up to 4 per cent in half-eunuchs and 9 per cent in full-eunuchs through emasculation, endurance increases significantly in half-eunuchs (32%) and particularly strongly in full-eunuchs (80%). Our results corroborate the gloves-off hypothesis and further point towards the adaptive significance of male emasculation.