Benefits of Pair-Bond Duration on Reproduction in a Lifelong Monogamous Cooperative Passerine.

AbstractLong-term social and genetic monogamy is rare in animals except birds, but even in birds it is infrequent and poorly understood. We investigated possible advantages of monogamy in a colonial, facultative cooperatively breeding bird from an arid, unpredictable environment, the sociable weaver (Philetairus socius). We documented divorce and extrapair paternity of 703 pairs over 10 years and separated effects of pair duration from breeding experience by analyzing longitudinal and cross-sectional datasets. Parts of the colonies were protected from nest predation, thereby limiting its stochastic and thus confounding effect on fitness measures. We found that 6.4% of sociable weaver pairs divorced and 2.2% of young were extrapair. Longer pair-bonds were associated with more clutches and fledglings per season and with reproducing earlier and later in the season, when snake predation is lower, but not with increased egg or fledgling mass or with nestling survival. Finally, the number of helpers at the nest increased with pair-bond duration. Results were similar for protected and unprotected nests. We suggest that long-term monogamy is associated with a better capacity for exploiting a temporally unpredictable environment and helps to form larger groups. These results can contribute to our understanding of why long-term monogamy is frequently associated with unpredictable environments and cooperation.

Interplay of cooperative breeding and predation risk on egg allocation and reproductive output.

Predation risk can influence behavior, reproductive investment, and, ultimately, individuals' fitness. In high-risk environments, females often reduce allocation to reproduction, which can affect offspring phenotype and breeding success. In cooperative breeders, helpers contribute to feed the offspring, and groups often live and forage together. Helpers can, therefore, improve reproductive success, but also influence breeders' condition, stress levels and predation risk. Yet, whether helper presence can buffer the effects of predation risk on maternal reproductive allocation remains unstudied. Here, we used the cooperatively breeding sociable weaver Philetairus socius to test the interactive effects of predation risk and breeding group size on maternal allocation to clutch size, egg mass, yolk mass, and yolk corticosterone. We increased perceived predation risk before egg laying using playbacks of the adults' main predator, gabar goshawk (Micronisus gabar). We also tested the interactive effects of group size and prenatal predator playbacks on offspring hatching and fledging probability. Predator-exposed females laid eggs with 4% lighter yolks, but predator-calls' exposure did not clearly affect clutch size, egg mass, or egg corticosterone levels. Playback-treatment effects on yolk mass were independent of group size, suggesting that helpers' presence did not mitigate predation risk effects on maternal allocation. Although predator-induced reductions in yolk mass may decrease nutrient availability to offspring, potentially affecting their survival, playback-treatment effects on hatching and fledging success were not evident. The interplay between helper presence and predator effects on maternal reproductive investment is still an overlooked area of life history and physiological evolutionary trade-offs that requires further studies.

Egg components and offspring survival vary with group size and laying order in a cooperative breeder.

Prenatal resource allocation to offspring can be influenced by maternal environment and offspring value, and affect offspring survival. An important pathway for flexible maternal allocation is via egg components such as nutrients and hormones. In cooperative breeders, females with helpers may increase resource allocation to eggs-'differential allocation'-or reduce it-'load-lightening'. Yet, helper effects on egg composition have been poorly studied. Moreover, it is unknown how helpers' presence modulates laying order effects on egg content and survival. Here, we investigated how maternal allocation varied with group size and laying order in the cooperatively breeding sociable weaver (Philetairus socius). We estimated interactive effects of helpers and laying order on allocation to egg mass, yolk nutrients-yolk mass, proteins, lipids, carotenoids, vitamin A and vitamin E-and hormones-testosterone, androstenedione, and corticosterone. Results concurred with the 'differential allocation' predictions. Females with more helpers produced later-laid eggs with heavier yolks and more lipids, and laid eggs overall richer in lipids. Proteins, antioxidants, and hormones were not found to vary with helper number. We then analyzed how helper number modulated laying order effects on survival. Females with more helpers did not specifically produce later-laid eggs with higher survival, but eggs laid by females with more helpers were overall more likely to fledge. These findings show that some egg components (yolk mass, lipids) can positively vary according to females' breeding group size, which may improve offspring fitness.

Strength of the 'island rule' in birds is positively associated with absence of avian predators.

The similar characteristics shared by island environments have been shown to lead to common patterns of adaptations in island species, commonly referred to as the 'insularity syndrome'. A well-known example is the 'island rule', where large species become smaller on islands and small species become larger, leading to well-known cases of dwarfism and gigantism. This pattern was recently verified on a global scale, but the mechanisms underlying it have been poorly investigated. Here, we focused on the role of released pressure from predation and competition experienced by island birds. Using 120 pairs of endemic island species and their mainland sister relatives, we first verified that the island rule was detected in our dataset, and then evaluated the effects of the numbers of raptors and interspecific competitors on the evolution of the insular species' body mass. We found a strong effect of predation on body mass evolution, with a stronger island rule for species occurring on islands with no raptors, while the pattern disappears in their presence. However, we did not find an effect of competition on this pattern. Our study shows the importance of considering ecological interactions for understanding patterns of body size evolution, and the exceptions to those patterns.

Evolution of female colours in birds: The role of female cost of reproduction and paternal care.

Female ornamentation is frequently observed in animal species and is sometimes found as more evolutionary labile than male ornamentation. A complex array of factors may explain its presence and variation. Here we assessed the role of female cost of reproduction and paternal care. Both factors have been pinpointed as important by theoretical studies but have not been investigated yet in details at the interspecific level. We worked on 133 species of North temperate Passeriformes bird species for which both the clutch volume - here taken as the proxy of female cost of reproduction - and amount of paternal care are relatively well known. Using spectrometry, we measured the whole-body coloured plumage patches and quantified three metrics corresponding to brightness (i.e. achromatic component), colour chromaticity (i.e. intensity) and colour volume (i.e. diversity). We found a strong association between male and female colour metrics. Controlling for this association, we found additional small but detectable effects of both cost of reproduction and paternal care. First, females of species with more paternal care were slightly brighter. Second, the interaction between the level of paternal care and egg volume was correlated with female colour intensity: females with more paternal care were more chromatic, with this association mostly present when their investment in reproduction was low. Together these results suggest that female cost of reproduction and paternal care are part of the multiple factors explaining variation of female coloration, besides the strong covariation between male and female coloration.

Long-Term Decrease in Coloration: A Consequence of Climate Change?

AbstractClimate change has been shown to affect fitness-related traits in a wide range of taxa; for instance, warming leads to phenological advancements in many plant and animal species. The influence of climate change on social and secondary sexual traits, which are associated with fitness because of their role as quality signals, is, however, unknown. Here, we use more than 5,800 observations collected on two Mediterranean blue tit subspecies (Cyanistes caeruleus caeruleus and Cyanistes caeruleus ogliastrae) to explore whether blue crown and yellow breast patch colorations have changed over the past 15 years. Our data suggest that coloration has become duller and less chromatic in both sexes. In addition, in the Corsican C.c. ogliastrae, but not in the mainland C.c. caeruleus, the decrease is associated with an increase in temperature at molt. Quantitative genetic analyses do not reveal any microevolutionary change in the color traits over the study period, strongly suggesting that the observed change over time was caused by a plastic response to the environmental conditions. Overall, this study suggests that ornamental colorations could become less conspicuous because of warming, revealing climate change effects on sexual and social ornaments and calling for further research on the proximate mechanisms behind these effects.

Differences in the temporal scale of reproductive investment across the slow-fast continuum in a passerine.

Life-history strategies differ with respect to investment in current versus 'future' reproduction, but when is this future? Under the novel 'temporality in reproductive investment hypothesis', we postulate variation should exist in the time frame over which reproductive costs are paid. Slow-paced individuals should pay reproductive costs over short (e.g. inter-annual) time scales to prevent reproductive costs accumulating, whereas fast-paced individuals should allow costs to accumulate (i.e. senescence). Using Fourier transforms, we quantify adjustments in clutch size with age, across four populations of blue tits (Cyanistes caeruleus). Fast populations had more prevalent and stronger long-term changes in reproductive investment, whereas slower populations had more prevalent short-term adjustments. Inter-annual environmental variation partly accounted for short-, but not long-term changes in reproductive investment. Our study reveals individuals differ in when they pay the cost of reproduction and that failure to partition this variation across different temporal scales and environments could underestimate reproductive trade-offs.

Disentangling climatic and nest predator impact on reproductive output reveals adverse high-temperature effects regardless of helper number in an arid-region cooperative bird.

Climate exerts a major influence on reproductive processes, and an understanding of the mechanisms involved and which factors might mitigate adverse weather is fundamental under the ongoing climate change. Here, we study how weather and nest predation influence reproductive output in a social species, and examine whether larger group sizes can mitigate the adverse effects of these factors. We used a 7-year nest predator-exclusion experiment on an arid-region cooperatively breeding bird, the sociable weaver. We found that dry and, especially, hot weather were major drivers of nestling mortality through their influence on nest predation. However, when we experimentally excluded nest predators, these conditions were still strongly associated with nestling mortality. Group size was unimportant against nest predation and, although positively associated with reproductive success, it did not mitigate the effects of adverse weather. Hence, cooperative breeding might have a limited capacity to mitigate extreme weather effects.

Patterns of bird song evolution on islands support the character release hypothesis in tropical but not in temperate latitudes.

The character release hypothesis-which predicts that a decline in interspecific competition leads to the expansion of trait expression-remains to be tested for communication signals. Taking advantage of the fact that oceanic islands host fewer species than the mainland, we tested whether island birds show an increase in frequency bandwidth of acoustic signals compared with mainland birds. Given the higher animal diversity and more saturated acoustic space in the tropics, we expected acoustic character release, if any, to be stronger in the tropics than in the temperate zone. We field recorded 22 bird species (11 pairs consisting of an endemic island species and its closest mainland relative) breeding at similar latitudes and in similar habitats: six tropical pairs (São Tomé Island/Mount Cameroon) and five temperate pairs (Madeira Island/southern France). For each species, we measured the degree of acoustic interference experienced when vocalizing and the spectral characteristics of its song (minimum and maximum frequencies, bandwidth). As expected, island species spent more time vocalizing alone, and any overlap in vocalizations involved fewer species. The vocalizations of island species spanned broader frequency bandwidths than their mainland counterparts in the tropics (true for all six pairs), but this pattern was less evident in the temperate region (2/5 pairs with no marked differences and 1/5 with opposite pattern). Overall, the character release of communication signals only occurred where the differential in number of species was large (tropics). We discuss latitude differences and the potential factors driving the observed differences.

Contrasting associations between nestling telomere length and pre and postnatal helpers' presence in a cooperatively breeding bird.

Studies on cooperative breeders have addressed the effects of non-breeding 'helpers' on reproduction and parental care, but the consequences for offspring physiology and long-term survival are less understood. Helpers are expected to benefit offspring, but their presence can also lead to decreased pre- or post-natal parental reproductive effort. To examine whether prenatal and postnatal helpers influence offspring condition, we conducted a whole-clutch cross-fostering experiment in sociable weavers (Philetairus socius) that altered the nestlings' social environment (presence/absence of helpers). We tested whether relative telomere length (rTL), an indicator of somatic maintenance, was influenced by prenatal and/or postnatal presence of helpers 9 and 17 days after hatching, and whether rTL predicted long-term survival. Nine days after hatching, we found an overall positive effect of postnatal helpers on rTL: for nestlings with prenatal helpers, a reduction in the number of helpers post-hatch was associated with shorter telomeres, while nestlings swapped from nests without helpers to nests with helpers had a larger rTL. However, when prenatal helpers were present, an increased number of helpers after hatching led to shorter telomeres. Nine-day old chicks with longer rTL tended to be more likely to survive over the 5 years following hatching. However, close to fledging, there was no detectable effect of the experiment on rTL and no link between rTL and survival. This experimental study of a wild cooperative breeder, therefore, presents partial support for the importance of the presence of helpers for offspring rTL and the link between early-life telomere length and long-term survival.

Maternal allocation in relation to weather, predation and social factors in a colonial cooperative bird.

Females may adjust prenatal allocation in relation to ecological conditions that affect reproductive success, such as weather conditions or predation risk. In cooperative breeders, helpers might also influence reproductive success, and previous studies suggest that females can lay smaller eggs or larger clutches when breeding with more helpers. Although recent work suggests that helper effects can vary according to climatic variables, how social and ecological factors interact to shape prenatal allocation is poorly understood. Here, we examine how ecological and social components of the breeding environment covary with egg mass and clutch size, using as a model the sociable weaver Philetairus socius, a colonial, cooperatively breeding passerine. The study spanned 9 years and included over 1,900 eggs from over 550 clutches. Our analyses combined natural variation in weather conditions (rainfall before each reproductive event) with a nest predator-exclusion experiment and continuous monitoring of the mother's social environment, allowing us to estimate how individual females adjust allocation to reproduction as their number of helpers varies. We found that egg mass varied consistently within females and did not clearly differ in relation to rainfall or predation risk. Contrary to previous studies, there was no evidence for plastic adjustments as females gained and lost helpers, and egg mass was instead better predicted by mother size and identity. Females laid larger clutches when breeding in environments where predation risk was experimentally reduced and after higher rainfall levels. Yet, there was no evidence for increasing clutch size as the number of helpers increased, nor for an interaction between helper effects and ecological factors. We conclude that while sociable weaver females can vary their clutch size, they show high individual consistency in egg mass. In addition, we found no evidence that females may maximize fitness through plastic prenatal allocation in relation to the number of helpers, or that the presence/absence of helper effects is modulated by rainfall levels or predation risk. These results challenge our current knowledge on some of the possible benefits of breeding with helpers and call for more long-term analyses on reproductive allocation adjustments in other cooperative systems.

Connecting the data landscape of long-term ecological studies: The SPI-Birds data hub.

The integration and synthesis of the data in different areas of science is drastically slowed and hindered by a lack of standards and networking programmes. Long-term studies of individually marked animals are not an exception. These studies are especially important as instrumental for understanding evolutionary and ecological processes in the wild. Furthermore, their number and global distribution provides a unique opportunity to assess the generality of patterns and to address broad-scale global issues (e.g. climate change). To solve data integration issues and enable a new scale of ecological and evolutionary research based on long-term studies of birds, we have created the SPI-Birds Network and Database (www.spibirds.org)-a large-scale initiative that connects data from, and researchers working on, studies of wild populations of individually recognizable (usually ringed) birds. Within year and a half since the establishment, SPI-Birds has recruited over 120 members, and currently hosts data on almost 1.5 million individual birds collected in 80 populations over 2,000 cumulative years, and counting. SPI-Birds acts as a data hub and a catalogue of studied populations. It prevents data loss, secures easy data finding, use and integration and thus facilitates collaboration and synthesis. We provide community-derived data and meta-data standards and improve data integrity guided by the principles of Findable, Accessible, Interoperable and Reusable (FAIR), and aligned with the existing metadata languages (e.g. ecological meta-data language). The encouraging community involvement stems from SPI-Bird's decentralized approach: research groups retain full control over data use and their way of data management, while SPI-Birds creates tailored pipelines to convert each unique data format into a standard format. We outline the lessons learned, so that other communities (e.g. those working on other taxa) can adapt our successful model. Creating community-specific hubs (such as ours, COMADRE for animal demography, etc.) will aid much-needed large-scale ecological data integration.

How to make methodological decisions when inferring social networks.

Social network analyses allow studying the processes underlying the associations between individuals and the consequences of those associations. Constructing and analyzing social networks can be challenging, especially when designing new studies as researchers are confronted with decisions about how to collect data and construct networks, and the answers are not always straightforward. The current lack of guidance on building a social network for a new study system might lead researchers to try several different methods and risk generating false results arising from multiple hypotheses testing. Here, we suggest an approach for making decisions when starting social network research in a new study system that avoids the pitfall of multiple hypotheses testing. We argue that best edge definition for a network is a decision that can be made using a priori knowledge about the species and that is independent from the hypotheses that the network will ultimately be used to evaluate. We illustrate this approach with a study conducted on a colonial cooperatively breeding bird, the sociable weaver. We first identified two ways of collecting data using different numbers of feeders and three ways to define associations among birds. We then evaluated which combination of data collection and association definition maximized (a) the assortment of individuals into previously known "breeding groups" (birds that contribute toward the same nest and maintain cohesion when foraging) and (b) socially differentiated relationships (more strong and weak relationships than expected by chance). This evaluation of different methods based on a priori knowledge of the study species can be implemented in a diverse array of study systems and makes the case for using existing, biologically meaningful knowledge about a system to help navigate the myriad of methodological decisions about data collection and network inference.

Examining the link between relaxed predation and bird coloration on islands.

Insular ecosystems share analogous ecological conditions, leading to patterns of convergent evolution that are collectively termed as the 'island syndrome'. In birds, part of this syndrome is a tendency for a duller plumage, possibly as a result of relaxed sexual selection. Despite this global pattern, some insular species display a more colourful plumage than their mainland relatives, but why this occurs has remained unexplained. Here, we examine the hypothesis that these cases of increased plumage coloration on islands could arise through a relaxation of predation pressure. We used comparative analyses to investigate whether average insular richness of raptors of suitable mass influences the plumage colourfulness and brightness across 110 pairs of insular endemic species and their closest mainland relatives. As predicted, we find a likely negative relationship between insular coloration and insular predation while controlling for mainland predation and coloration, suggesting that species were more likely to become more colourful as the number of insular predators decreased. By contrast, plumage brightness was not influenced by predation pressure. Relaxation from predation, together with drift, might thus be a key mechanism of species phenotypic responses to insularity.

Testing the Sexual and Social Benefits of Cooperation in Animals.

Theoretical models show that sexual and social selection can stabilise cooperation. However, field tests of these mechanisms have been difficult to conduct and the results are mixed. We discuss the conceptual and practical difficulties associated with testing the role of social and sexual selection on cooperation and argue that there are alternative ways of examining these hypotheses. Specifically, approaches based on the classic theories of sexual selection and signalling, and recent developments in the field of behavioural syndromes, provide mechanisms to insure the reliability of cooperation. In addition, methodological developments (social networks and microtracking) and long-term datasets, allow measuring partner choice in a cooperation context and the resulting fitness benefits for both the cooperators and the individuals that associate with them.

Insularity effects on the assemblage of the blood parasite community of the birds from the Gulf of Guinea.

AIM: Lower species diversity, increased population densities and ecological niche enlargement are common characteristics of island faunas. However it remains to be determined if they extend to the parasite community. We tested if Haemosporidia parasite pressure varies between islands and the mainland with two different levels of analysis: i) at the host community level, and ii) with paired-species comparisons between islands and the mainland. LOCATION: Gulf of Guinea, West Africa. METHODS: We used molecular-based methods to identify avian Haemosporidian parasites (Plasmodium, Haemoproteus and Leucocytozoon) to describe their diversity, prevalence, host specificity and their phylogenetic relationships in five islands of the Gulf of Guinea and in nearby mainland areas. RESULTS: We found reduced Haemosporidia diversity on islands for Haemoproteus and Leucocytozoon, but not for Plasmodium. In addition, lower parasite prevalence on islands was found using a paired-species approach. Although the mean host specificity of the parasite community on islands did not differ from the mainland, we found a very distinct parasite species assemblage on the islands, which was composed of both the most generalist and the most specialist lineages. MAIN CONCLUSIONS: This study supports the hypothesis that parasite pressure is reduced on islands. Colonization is made by generalists with high host switching capacities, with some subsequently evolving into highly specialised parasites. This suggests that 'taxon cycle' dynamics may explain the assemblage of insular parasite communities.

Breeding decisions and output are correlated with both temperature and rainfall in an arid-region passerine, the sociable weaver.

Animal reproductive cycles are commonly triggered by environmental cues of favourable breeding conditions. In arid environments, rainfall may be the most conspicuous cue, but the effects on reproduction of the high inter- and intra-annual variation in temperature remain poorly understood, despite being relevant to the current context of global warming. Here, we conducted a multiyear examination of the relationships between a suite of measures of temperature and rainfall, and the onset and length of the breeding season, the probability of breeding and reproductive output in an arid-region passerine, the sociable weaver (Philetairus socius). As expected, reproductive output increased with rainfall, yet specific relationships were conditional on the timing of rainfall: clutch production was correlated with rainfall throughout the season, whereas fledgling production was correlated with early summer rainfall. Moreover, we reveal novel correlations between aspects of breeding and temperature, indicative of earlier laying dates after warmer springs, and longer breeding seasons during cooler summers. These results have implications for understanding population trends under current climate change scenarios and call for more studies on the role of temperature in reproduction beyond those conducted on temperate-region species.

Insularity effects on bird immune parameters: A comparison between island and mainland populations in West Africa.

Oceanic islands share several environmental characteristics that have been shown to drive convergent evolutionary changes in island organisms. One change that is often assumed but has seldom been examined is the evolution of weaker immune systems in island species. The reduction in species richness on islands is expected to lead to a reduced parasite pressure and, given that immune function is costly, island animals should show a reduced immune response. However, alternative hypotheses exist; for example, the slower pace of life on islands could favor the reorganization of the immune system components (innate vs. acquired immunity) on islands. Thus far, few island species have been studied and no general patterns have emerged. Here, we compared two immune parameters of birds from São Tomé and Príncipe islands to those of their close relatives at similar latitudes on the mainland (Gabon, West Africa). On islands, the acquired humoral component (total immunoglobulins) was lower for most species, whereas no clear pattern was detected for the innate component (haptoglobin levels). These different responses did not seem to arise from a reorganization of the two immune components, as both total immunoglobulins and haptoglobin levels were positively associated. This work adds to the few empirical studies conducted so far which suggest that changes in immune parameters in response to insularity are not as straightforward as initially thought.

Assortative mating by colored ornaments in blue tits: space and time matter.

Assortative mating is a potential outcome of sexual selection, and estimating its level is important to better understand local adaptation and underlying trait evolution. However, assortative mating studies frequently base their conclusions on small numbers of individuals sampled over short periods of time and limited spatial scales even though spatiotemporal variation is common. Here, we characterized assortative mating patterns over 10 years in four populations of the blue tit (Cyanistes caeruleus), a passerine bird. We focused on two plumage ornaments-the blue crown and the yellow breast patch. Based on data for 1,657 pairs of birds, we found large interannual variation: assortative mating varied from positive to negative. To determine whether there was nonetheless a general trend in the data, we ran a within-study meta-analysis. It revealed that assortative mating was moderately positive for both ornaments. It also showed that mating patterns differed among populations and especially between two neighboring populations that displayed phenotypic divergence. Our results therefore underscore that long-term studies are needed to draw broad conclusions about mating patterns in natural populations. They also call for studying the potential role of assortative mating in local adaptation and evolution of ornaments in both sexes.