Sjouke A. Kingma

Radical loss of an extreme extra-pair mating system

BackgroundMating outside the pair-bond is surprisingly common in socially monogamous birds, but rates of extra-pair paternity (EPP) vary widely between species. Although differences in life-history and contemporary ecological factors may explain some interspecific variation, evolutionary forces driving extra-pair (EP) mating remain largely obscure. Also, since there is a large phylogenetic component to the frequency of EPP, evolutionary inertia may contribute substantially to observed EP mating patterns. However, the relative importance of plasticity and phylogenetic constraints on the incidence of EP mating remains largely unknown.ResultsWe here demonstrate very low levels of EPP (4.4% of offspring) in the purple-crowned fairy-wren Malurus coronatus, a member of the genus with the highest known levels of EPP in birds. In addition, we show absence of the suite of distinctive behavioral and morphological adaptations associated with EP mating that characterize other fairy-wrens. Phylogenetic parsimony implies that these characteristics were lost in one speciation event. Nonetheless, many life-history and breeding parameters that are hypothesized to drive interspecific variation in EPP are not different in the purple-crowned fairy-wren compared to its promiscuous congeners.ConclusionSuch radical loss of an extreme EP mating system with all associated adaptations from a lineage of biologically very similar species indicates that evolutionary inertia does not necessarily constrain interspecific variation in EPP. Moreover, if apparently minor interspecific differences regularly cause large differences in EPP, this may be one reason why the evolution of EP mating is still poorly understood.

Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity?

1. Kin selection is one of the mechanisms that can explain apparent altruism by subordinate individuals in cooperatively breeding species, if subordinates boost the production of kin. We compared productivity and breeder survival in pairs with and without subordinates in a genetically monogamous cooperatively breeding bird, the purple-crowned fairy-wren Malurus coronatus. 2. Additive effects of subordinate help increased productivity. Total feeding rates to the nest were increased by two or more subordinates, and fledgling production was greater in larger groups. Not all subordinates contributed to nestling feeding, and the effect of group size was greater when non-contributors were excluded from analyses, suggesting that increased fledgling production was a direct result of help. 3. Compensatory effects of subordinate help improved breeder survival. Assisted breeders reduced their workload by 20-30%, irrespective of the number of helpers. Although re-nesting intervals were not affected by group size, reduced breeder feeding rates resulted in improved survival and breeders in larger groups survived better. 4. Subordinates and nestlings are usually progeny of the breeding pair in this species, and benefits of cooperative breeding are very different from three congeners with extremely high levels of extra-group paternity (EGP). In these Malurus, fledgling production and survival of male breeders are not enhanced in larger groups. This is consistent with the expectation that kin-selected benefits vary with relatedness, and thus levels of EGP. 5. We tested whether benefits of cooperative breeding in 37 avian species varied with levels of extra-group mating. Both direct and phylogenetically controlled comparisons showed that improvement of (male) breeder survival and enhanced productivity are more likely when fidelity is higher, as predicted when investment of subordinates correlates with relatedness to offspring. This pattern highlights the importance of considering the genetic mating system for understanding the evolution of cooperative breeding.

Male songbird indicates body size with low-pitched advertising songs

Body size is a key sexually selected trait in many animal species. If size imposes a physical limit on the production of loud low-frequency sounds, then low-pitched vocalisations could act as reliable signals of body size. However, the central prediction of this hypothesis – that the pitch of vocalisations decreases with size among competing individuals – has limited support in songbirds. One reason could be that only the lowest-frequency components of vocalisations are constrained, and this may go unnoticed when vocal ranges are large. Additionally, the constraint may only be apparent in contexts when individuals are indeed advertising their size. Here we explicitly consider signal diversity and performance limits to demonstrate that body size limits song frequency in an advertising context in a songbird. We show that in purple-crowned fairy-wrens, Malurus coronatus coronatus, larger males sing lower-pitched low-frequency advertising songs. The lower frequency bound of all advertising song types also has a significant negative relationship with body size. However, the average frequency of all their advertising songs is unrelated to body size. This comparison of different approaches to the analysis demonstrates how a negative relationship between body size and song frequency can be obscured by failing to consider signal design and the concept of performance limits. Since these considerations will be important in any complex communication system, our results imply that body size constraints on low-frequency vocalisations could be more widespread than is currently recognised.

Differential deposition of antimicrobial proteins in blue tit (Cyanistes caeruleus) clutches by laying order and male attractiveness.

Female birds can influence offspring fitness by varying the relative quantities of egg components they deposit within and between clutches. Antimicrobial proteins (lysozyme, ovotransferrin, and avidin) are significant components of the avian albumen and likely aid in defense of embryos from microbial infection. Within clutches, females may enhance antimicrobial defense of early-laid eggs to protect them from the high risk of infection incurred before the onset of incubation. Among entire clutches, females may invest more resources in young sired by more attractive males because they have higher reproductive value. We tested these hypotheses by quantifying antimicrobial protein distribution within and among clutches in blue tit eggs. Contrary to our hypothesis, clutches showed no differential deposition of lysozyme or avidin within clutches, but eggs laid in the middle of the sequence had higher concentrations of ovotransferrin than eggs in the beginning and end. Consistent with our second hypothesis, we found that females produced eggs with higher concentrations of lysozyme (although not ovotransferrin or avidin) when mated to more attractive (more UV-reflective) males. Furthermore, females mated to polygynous males deposited less lysozyme than those mated to monogamous males. These data suggest that allocation of lysozyme at the clutch level may be a maternal effect mediated by male qualities.

Sexual selection and the function of a melanin-based plumage ornament in polygamous penduline tits Remiz pendulinus

Melanin-based ornaments are often involved in signaling aggression and dominance, and their role in sexual selection is increasingly recognized. We investigated the functions of a melanin-based plumage ornament (facial ‘mask’) in male Eurasian penduline tits Remiz pendulinus in the contexts of male–male aggression, mating success, and parental care. The penduline tit is a passerine bird with a unique mating system in which both sexes may mate with several mates in a breeding season, and one (or both) parent deserts the clutch. Our study revealed that mask size of males is more likely an honest signal used by females in their mate choice decisions than a trait involved in male–male competition. First, mask size increased with both age and body condition, indicating that the mask may signal male quality. Second, males with larger masks paired more quickly and had more mates over the breeding season than males with smaller masks. Third, we found no evidence that male mask size signals male–male aggression or dominance during competitive encounters. The increased mating success of large-masked males, however, did not translate into higher reproductive success, as nestling survival decreased with mask size. Therefore, we conclude that there is either no directional selection on male mask size or males with larger masks receive indirect, long-term benefits.

Multiple Benefits Drive Helping Behavior in a Cooperatively Breeding Bird: An Integrated Analysis

Several hypotheses exist to explain the seemingly altruistic helping behavior of cooperative breeders, although the general utility of these hypotheses remains unclear. While the potential importance of inclusive fitness benefits (kin selection) is traditionally widely appreciated, it is increasingly recognized that direct benefits may be more important than assumed. We use an integrative two-step framework to assess support for current hypotheses in purple-crowned fairy wrens, a species where subordinates vary in relatedness to breeders and helping increases productivity. After establishing that assumptions of pay-to-stay and social prestige hypotheses (predicting that helping functions as “paying rent” to stay on the territory or as a signal of individual quality, respectively) were not met and that parentage by subordinates is extremely rare, we tested whether subordinates adjusted nestling feeding rates following the predictions of the kin selection and group augmentation hypotheses. Benefits of kin selection result from investment in relatives, and group augmentation benefits accrue when subordinates invest more in their own future helpers, for example, when they have a better chance of inheriting the breeding position. We found that subordinates fed siblings more than unrelated nestlings, indicating that kin selection could facilitate cooperation. Moreover, the effect of relatedness on feeding effort varied depending on the probability of inheriting a breeding position, suggesting that active group augmentation can explain investment by unrelated subordinates. This statistical interaction would have gone undetected had we not considered both factors simultaneously, illustrating that a focus on single hypotheses could lead to underestimation of their importance in explaining cooperative breeding.

Senescence in the wild: Insights from a long-term study on Seychelles warblers.

Senescence--the progressive age-dependent decline in performance--occurs in most organisms. There is considerable variation in the onset and rate of senescence between and within species. Yet the causes of this variation are still poorly understood, despite being central to understanding the evolution of senescence. Long-term longitudinal studies on wild animals are extremely well-suited to studying the impact of environmental and individual characteristics (and the interaction between the two) on senescence, and can help us to understand the mechanisms that shape the evolution of senescence. In this review, we summarize and discuss the insights gained from our comprehensive long-term individual-based study of the Seychelles warbler (Acrocephalus sechellensis). This species provides an excellent model system in which to investigate the evolution of senescence in the wild. We found that Seychelles warblers show senescent declines in survival and reproduction, and discuss how individual characteristics (body condition, body size) and environmental effects (low- versus high-quality environments) may affect the onset and rate of senescence. Further, we highlight the evidence for trade-offs between early-life investment and senescence. We describe how key cellular and physiological processes (oxidative stress and telomere shortening) underpinning senescence are affected by individual and environmental characteristics in the Seychelles warbler (e.g. food availability, reproductive investment, disease) and we discuss how such physiological variation may mediate the relationship between environmental characteristics and senescence. Based on our work using Seychelles warblers as a model system, we show how insights from long-term studies of wild animals may help unravel the causes of the remarkable variation in senescence observed in natural systems, and highlight areas for promising future research.

Melatonin delays clutch initiation in a wild songbird

The hormone melatonin is known to play an important role in regulating many seasonal changes in physiology, morphology and behaviour. In birds, unlike in mammals, melatonin has thus far been thought to play little role in timing seasonal reproductive processes. This view is mainly derived from laboratory experiments on male birds. This study tests whether melatonin is capable of influencing the timing of clutch initiation in wild female songbirds. Free-living female great tits (Parus major) treated with melatonin-filled implants prior to the breeding season initiated their first clutch of the season significantly later than females carrying an empty implant. Melatonin treatment did not affect clutch size. Further, melatonin treatment did not delay the onset of daily activity in the wild nor adversely affect body mass in captivity compared with controls. These data suggest a previously unknown role for this hormone in regulating the timing of clutch initiation in the wild.

Costs of sleeping in: circadian rhythms influence cuckoldry risk in a songbird

Summary Circadian (i.e. daily) regulation of behaviours is thought to provide fitness benefits to organisms by enabling them to anticipate diel changes in the environment, such as sunrise. A common behaviour among socially monogamous songbirds that usually takes place in the early mornings is extra-pair mating, that is copulating with partners outside of the social pair bond. Thus, variation in when individuals begin their daily activity may influence their reproductive success; early risers may be better able to gain copulations and guard their partners, thus minimizing their risk of being cuckolded compared with late risers. Sexual selection may thus play an important role in shaping circadian behaviours, but this assumption has yet to be tested in free-living animals. Here, we experimentally weakened endogenous circadian rhythmicity, and thus, anticipation of dawn in male great tits (Parus major) in the wild through the subcutaneous administration of implants filled with melatonin shortly before egg-laying began in this population. Melatonin is a hormone released during the dark phase at night and is one important cue animals use to entrain their circadian clock. Experimental individuals delayed the onset of daily activity compared with controls and were more likely to be cuckolded compared with control males. Manipulation did not alter other behavioural traits observed; no difference between treatments was observed in activity levels during the day or in the end time of daily activity. These results strongly support the assumption that selection, particularly sexual selection, shapes the circadian phenotypes of wild vertebrates which enable anticipation of important and predictive diel changes in an individuals biotic and abiotic environment.

Seasonal male plumage as a multi-component sexual signal: insights and opportunities

Abstract Seasonal breeding plumage of male fairy-wrens (Malurus spp.) shows significant inter-and intra-specific variation in several potential signalling components that we systematically review here. There is extensive colour variation in the genus, possibly related to variation in visual sensitivity. In many species, males can delay development of their first complete breeding plumage for one or more years, although males in more complete breeding plumage appear to be reproductively more successful. An additional sexual signal, and an evolutionary innovation, is the timing of the pre-breeding moult. A mechanism regulating this moult is testosterone, which can stimulate initiation of moult and development of male breeding colouration and is presumably required for maintenance of the breeding plumage. Males undertake pre-breeding moult earlier as they age, and early pre-breeding moult appears selected by female choice for extra-pair mates. Few studies have addressed variation in colour quality or the role of plumage in aggressive interactions. Condition-dependence of moult or breeding plumage has not been experimentally investigated. We argue that the genus is particularly suited to comparative analyses, as it provides informative contrasts in colour, plumage development, patterns of moult, colour vision and mating system, offering many exciting opportunities for testing evolutionary theories on function and maintenance of sexual signals.