Thomas W. Pike

Behavioural phenotype affects social interactions in an animal network

Animal social networks can be extremely complex and are characterized by highly non-random interactions between group members. However, very little is known about the underlying factors affecting interaction preferences, and hence network structure. One possibility is that behavioural differences between individuals, such as how bold or shy they are, can affect the frequency and distribution of their interactions within a network. We tested this using individually marked three-spined sticklebacks (Gasterosteus aculeatus), and found that bold individuals had fewer overall interactions than shy fish, but tended to distribute their interactions more evenly across all group members. Shy fish, on the other hand, tended to associate preferentially with a small number of other group members, leading to a highly skewed distribution of interactions. This was mediated by the reduced tendency of shy fish to move to a new location within the tank when they were interacting with another individual; bold fish showed no such tendency and were equally likely to move irrespective of whether they were interacting or not. The results show that animal social network structure can be affected by the behavioural composition of group members and have important implications for understanding the spread of information and disease in social groups.

Carotenoids, oxidative stress and female mating preference for longer lived males.

Some of the most spectacular exaggerated sexual ornaments are carotenoid dependent. It has been suggested that such ornaments have evolved because carotenoid pigments are limiting for both signal expression and in their role as antioxidants and immunostimulants. An implicit assumption of this hypothesis is that males which can afford to produce more elaborate carotenoid-dependent displays are signalling their enhanced ability to resist parasites, disease or oxidative stress and hence would be predicted to live longer. Therefore, in species with carotenoid-dependent ornaments where a parents future longevity is crucial for determining offspring survival, there should be a mating preference for partners that present the lowest risk of mortality during the breeding attempt, as signalled by the ability to allocate carotenoids to sexual displays. In an experimental study using three-spined sticklebacks (Gasterosteus aculeatus), we show that when dietary carotenoid intake is limited, males attempt to maintain their sexual ornament at the expense of body carotenoids and hence suffer from reduced reproductive investment and a shorter lifespan. These males also suffer from an increased susceptibility to oxidative stress, suggesting that this may constitute the mechanism underlying the increased rate of ageing. Furthermore, in pairwise mate-choice trials, females preferred males that had a greater access to carotenoids and chance of surviving the breeding season, suggesting that females can make adaptive mate choice decisions based on a males carotenoid status and potential future longevity.

Availability of non-carotenoid antioxidants affects the expression of a carotenoid-based sexual ornament.

Carotenoids are responsible for much of the yellow, orange and red pigmentation in the animal kingdom, and the importance of such coloration as an honest signal of individual quality has received widespread attention. In particular, owing to the multiple roles of carotenoids as pigments, antioxidants and immunostimulants, carotenoid-based coloration has been suggested to advertise an individuals antioxidant or immune defence capacity. However, it has recently been argued that carotenoid-based signals may in fact be advertising the availability of different antioxidants, many of which (including various vitamins, antioxidant enzymes and minerals) are colourless and so would be uninformative as components of a visual signal, yet often have greater biological activity than carotenoids. We tested this hypothesis by feeding male sticklebacks (Gasterosteus aculeatus) a diet containing a fixed level of carotenoids and either low or high, but biologically realistic levels of the colourless antioxidant vitamins C and E. High-antioxidant diet males produced significantly more intensely coloured (but not larger) carotenoid-based regions of nuptial coloration and were preferred over size-matched males of the opposite diet treatment in mate-choice trials. Furthermore, there were positive correlations between an individuals somatic antioxidant activity and signal intensity. Our data suggest that carotenoid-based ornaments may honestly signal an individuals availability of non-carotenoid antioxidants, allowing females to make adaptive mate-choice decisions.

Dietary carotenoid availability, sexual signalling and functional fertility in sticklebacks

In species where males express carotenoid-based sexual signals, more intensely coloured males may be signalling their enhanced ability to combat oxidative stress. This may include mitigating deleterious oxidative damage to their sperm, and so be directly related to their functional fertility. Using a split-clutch in vitro fertilization technique and dietary carotenoid manipulation, we demonstrate that in non-competitive fertilization assays, male three-spined sticklebacks (Gasterosteus aculeatus) that are fed higher (but biologically relevant) levels of carotenoids had a significantly increased fertilization success, irrespective of maternal carotenoid intake. Furthermore, within diet groups, a males fertilization success was positively related to the expression of his carotenoid-based nuptial coloration, with more intensely coloured males having higher functional fertility. These data provide, to our knowledge, the first demonstration that dietary access to carotenoids influences fertilization success, and suggest that females could use a males nuptial coloration as an indicator of his functional fertility.

Offspring sex ratio is related to paternal train elaboration and yolk corticosterone in peafowl

Several recent experimental studies have provided strong evidence for the ability of birds to manipulate the sex ratio of their offspring prior to laying. Using a captive population of peafowl (Pavo cristatus), we tested experimentally the effects of paternal attractiveness on offspring sex ratio, and related sex ratio deviations to egg-yolk concentrations of testosterone, 17β-estradiol and corticosterone. When females were mated to males whose attractiveness had been experimentally reduced by removing prominent eyespot feathers from their trains, they produced significantly more female offspring, had significantly higher yolk corticosterone concentrations and tended to have lower levels of yolk testosterone than when mated to the same males with their full complement of feathers. Concentrations of 17β-estradiol did not vary consistently with sex ratio biases. These findings add to the small number of studies providing experimental evidence that female birds can control the primary sex ratio of their offspring in response to paternal attractiveness, and highlight the possibility that corticosterone and perhaps testosterone are involved in the sex manipulation process in birds.

Maternal body condition and plasma hormones affect offspring sex ratio in peafowl

In theory, females that can afford to do so may increase their fitness by investing in offspring of the sex with the greater probability of attaining high reproductive success. This has been observed in a wide variety of mammalian, reptilian and avian species although the proximate mechanism remains a mystery. Using a captive population of peafowl, Pavo cristatus, we investigated the relation between maternal quality, offspring sex ratio and plasma concentrations of the reproductive hormones testosterone and 17β-oestradiol and the principal avian stress hormone corticosterone. Each peacock was paired with three peahens that differed with respect to their relative body condition, creating a condition and dominance hierarchy within each pen and thus a situation in which we would predict investment in offspring to vary between hens. We found significant intercorrelations between maternal body condition (but not dominance rank or clutch size), maternal plasma levels of corticosterone and testosterone (but not 17β-oestradiol) and clutch sex ratio, such that good maternal condition, low plasma corticosterone and high levels of testosterone were associated with male biases in the sex ratio and increased investment in male eggs. The observed biases were probably present at laying, and thus add to the growing number of studies showing primary sex ratio adjustment in response to maternal body condition, and furthermore may indicate a role for corticosterone and testosterone in the avian sex manipulation process.

Using digital cameras to investigate animal colouration: estimating sensor sensitivity functions

Spectrophotometers allow the objective measurement of colour and as a result are rapidly becoming a key piece of equipment in the study of animal colouration; however, they also have some major limitations. For example, they can only record point samples, making it difficult to reconstruct topographical information, and they generally require subjects to be inanimate during measurement. Recently, the use of digital cameras has been explored as an alternative to spectrophotometry. In particular, this allows whole scenes to be captured and objectively converted to animal colour space, providing spatial (and potentially temporal) data that would be unobtainable using spectrophotometry; however, mapping between camera and animal colour spaces requires knowledge of the spectral sensitivity functions of the camera’s sensors. This information is rarely available, and making direct measures of sensor sensitivity can be prohibitively expensive, technically demanding and time-consuming. As a result, various methods have been developed in the engineering and computing sciences that allow sensor sensitivity functions to be estimated using only readily collected data on the camera’s response to a limited number of colour patches of known surface reflectance. Here, I describe the practical application of one such method and demonstrate how it allows the recovery of sensor sensitivities (including in the ultraviolet) with a high enough degree of accuracy to reconstruct whole images in terms of the quantal catches of an animal’s photoreceptors, with calculated values that closely match those determined from spectrophotometric measurements. I discuss the potential for this method to advance our understanding of animal colouration.

Size-dependent directed social learning in nine-spined sticklebacks

To forage efficiently in a patchy environment animals must make informed decisions concerning in which patches to forage, for which the behaviour of other animals often provides informative cues. However, other individuals may differ in the quality or relevance of information that they provide, and accordingly animals are expected to be selective with respect to whom they copy. Such selectivity may include the biasing of copying towards older, larger or more experienced conspecifics. We investigated whether the ability of nine-spined sticklebacks, Pungitius pungitius, to exploit public information, that is, to judge the relative profitability of food patches solely on the basis of the relative feeding activity of others, is influenced by their own body size and that of the individuals from whom they copy. Individual observer fish, classed as either small or large, were trained that two discrete foraging patches differed in their relative quality, one being rich and the other poor (‘personal information’). They then watched two shoals of either small or large demonstrator conspecifics feeding at the two patches (‘public information’), but with relative profitability of the patches reversed compared to training, before being given the opportunity to make a patch choice. The effectiveness of this public demonstration was clearly contingent on the size of the demonstrators, with subjects of both size classes copying the patch choice of large demonstrators significantly more than they copied the patch choice of small demonstrators. This study reinforces the view that animal social learning is directed along particular pathways, with individuals predisposed by selection to copy particular categories of individual differentially.

Optimization of Resource Allocation Can Explain the Temporal Dynamics and Honesty of Sexual Signals

In species in which males are free to dynamically alter their allocation to sexual signaling over the breeding season, the optimal investment in signaling should depend on both a male’s state and the level of competition he faces at any given time. We developed a dynamic optimization model within a game‐theoretical framework to explore the resulting signaling dynamics at both individual and population levels and tested two key model predictions with empirical data on three‐spined stickleback (Gasterosteus aculeatus) males subjected to dietary manipulation (carotenoid availability): (1) fish in better nutritional condition should be able to maintain their signal for longer over the breeding season, resulting in an increasingly positive correlation between nutritional status and signal (i.e., increasing signal honesty), and (2) female preference for more ornamented males should thus increase over the breeding season. Both predictions were supported by the experimental data. Our model shows how such patterns can emerge from the optimization of resource allocation to signaling in a competitive situation. The key determinants of the honesty and dynamics of sexual signaling are the condition dependency of male survival, the initial frequency distribution of nutritional condition in the male population, and the cost of signaling.

Sex ratio manipulation in response to maternal condition in pigeons: evidence for pre-ovulatory follicle selection

A number of recent reports have documented offspring sex ratio biases in birds. However, to date the potential mechanisms that have been put forward to explain the proximate basis for these deviations are entirely speculative. Using a captive population of domestic pigeons (Columba livia domestica), I tested the hypothesis that mothers in relatively poor physical condition should overproduce daughters by manipulating maternal body condition around the time of egg laying by continuous egg removal and differing feeding regimes. During treatment, females were fed a controlled quantity of food. This, combined with the high energetic costs of repeated egg production caused a significant reduction in maternal body weight. In contrast, during control when food was available ad libitum, maternal body weight did not decline, despite repeated egg production. No significant deviation from parity was evident in the sex ratio of either the first or second eggs during control, whereas during treatment a significant female bias was evident in not only the first egg, but also in the second egg. The absence of single-egg clutches, the rarity of infertile eggs and the lack of laying delays between eggs strongly suggests that the mechanism of sex ratio adjustment in pigeons occurs prior to ovulation. The highly skewed sex-distribution within the two-egg clutches and the unexpectedly large amount of variation in the yolk weight of eggs produced during treatment (but not control) are consistent with the expectations of pre-ovulatory selective resorption of ‘wrong’ sex ovarian follicles.