Eduardo S. A. Santos

Methodological issues and advances in biological meta-analysis

Meta-analysis has changed the way researchers conduct literature reviews not only in medical and social sciences but also in biological sciences. Meta-analysis in biological sciences, especially in ecology and evolution (which we refer to as ‘biological’ meta-analysis) faces somewhat different methodological problems from its counterparts in medical and social sciences, where meta-analytic techniques were originally developed. The main reason for such differences is that biological meta-analysis often integrates complex data composed of multiple strata with, for example, different measurements and a variety of species. Here, we review methodological issues and advancements in biological meta-analysis, focusing on three topics: (1) non-independence arising from multiple effect sizes obtained in single studies and from phylogenetic relatedness, (2) detecting and accounting for heterogeneity, and (3) identifying publication bias and measuring its impact. We show how the marriage between mixed-effects (hierarchical/multilevel) models and phylogenetic comparative methods has resolved most of the issues under discussion. Furthermore, we introduce the concept of across-study and within-study meta-analysis, and propose how the use of within-study meta-analysis can improve many empirical studies typical of ecology and evolution.

The costs of parental care: a meta-analysis of the trade-off between parental effort and survival in birds

A fundamental premise of life‐history theory is that organisms that increase current reproductive investment suffer increased mortality. Possibly the most studied life‐history phenotypic relationship is the trade‐off between parental effort and survival. However, evidence supporting this trade‐off is equivocal. Here, we conducted a meta‐analysis to test the generality of this tenet. Using experimental studies that manipulated parental effort in birds, we show that (i) the effect of parental effort on survival was similar across species regardless of phylogeny; (ii) individuals that experienced reduced parental effort had similar survival probabilities than control individuals, regardless of sex; and (iii) males that experienced increased parental effort were less likely to survive than control males, whereas females that experienced increased effort were just as likely to survive as control females. Our results suggest that the trade‐off between parental effort and survival is more complex than previously assumed. Finally, our study provides recommendations of unexplored avenues of future research into life‐history trade‐offs.

Dominance and plumage traits: meta-analysis and metaregression analysis

The study of avian signalling systems is an important avenue for research on animal communication. More specifically, the use of plumage traits to signal status or fighting ability has been extensively investigated for over 30 years. Yet, little is known about how strong and general the relationship between dominance and plumage traits is across different bird species. We conducted meta-analysis and metaregression analysis to investigate the relationship between dominance and plumage characteristics, using published literature on avian species. Our analyses tested possible moderators of this relationship, such as plumage trait and plumage colour, plumage manipulation, study location, type of dominance interaction, the use of model birds, type of dominance assessment and dominance context (breeding or nonbreeding). Our results revealed a significant effect size for the association between dominance and plumage. We found that the relationship between dominance and plumage was significantly influenced by the dominance assessment method used in the source study (direct or indirect). Furthermore, our analyses provide evidence that the role of plumage signalling may be similarly important during the breeding and nonbreeding seasons. We conclude that plumage signalling is a ubiquitous form of communicating status or fighting ability across bird species with different plumage types.

Mosaic-Level Inference of the Impact of Land Cover Changes in Agricultural Landscapes on Biodiversity: A Case-Study with a Threatened Grassland Bird

Changes in land use/land cover are a major driver of biodiversity change in the Mediterranean region. Understanding how animal populations respond to these landscape changes often requires using landscape mosaics as the unit of investigation, but few previous studies have measured both response and explanatory variables at the land mosaic level. Here, we used a “whole-landscape” approach to assess the influence of regional variation in the land cover composition of 81 farmland mosaics (mean area of 2900 ha) on the population density of a threatened bird, the little bustard (Tetrax tetrax), in southern Portugal. Results showed that ca. 50% of the regional variability in the density of little bustards could be explained by three variables summarising the land cover composition and diversity in the studied mosaics. Little bustard breeding males attained higher population density in land mosaics with a low land cover diversity, with less forests, and dominated by grasslands. Land mosaic composition gradients showed that agricultural intensification was not reflected in a loss of land cover diversity, as in many other regions of Europe. On the contrary, it led to the introduction of new land cover types in homogenous farmland, which increased land cover diversity but reduced overall landscape suitability for the species. Based on these results, the impact of recent land cover changes in Europe on the little bustard populations is evaluated.

Breeding Biology and Variable Mating System of a Population of Introduced Dunnocks (Prunella modularis) in New Zealand

Species with variable mating systems provide a unique opportunity to investigate whether females receive direct fitness benefits from additional male partners. The direct benefits provide an obvious explanation for why females would breed polyandrously, in a situation where males clearly do not attain their optimal reproductive success. Evidence for these direct benefits is, however, mixed. Here, we present a detailed study of the breeding biology of the dunnock, Prunella modularis, which inform an investigation into the effects of the social mating system on the reproductive success in a population of dunnocks in Southern New Zealand. We studied 80 different social groups over the course of three breeding seasons. Dunnocks in our population presented a variable mating system, with socially monogamous (45%), socially polyandrous (54%) and socially polygynandrous (1%) groups being observed in the same breeding season. We did not observe any polygynous social units in our study period although polygyny exists in the population. We found little difference in the numbers of eggs laid, and egg volume between monogamous and polyandrous nests. However, polyandrous groups had better hatching and fledging success than monogamous groups (composite d = 0.385, 95% CI: 0.307 to 0.463). Overall our results support the notion that polyandry is beneficial for females.

Population differentiation and behavioural association of the two ‘personality’ genes DRD4 and SERT in dunnocks (Prunella modularis)

Quantifying the variation in behaviour‐related genes within and between populations provides insight into how evolutionary processes shape consistent behavioural traits (i.e. personality). Deliberate introductions of non‐native species offer opportunities to investigate how such genes differ between native and introduced populations and how polymorphisms in the genes are related to variation in behaviour. Here, we compared the genetic variation of the two ‘personality’ genes, DRD4 and SERT, between a native (United Kingdom, UK) and an introduced (New Zealand, NZ) population of dunnocks, Prunella modularis. The NZ population showed a significantly lower number of single nucleotide polymorphisms (SNPs) compared to the UK population. Standardized F’st estimates of the personality genes and neutral microsatellites indicate that selection (anthropogenic and natural) probably occurred during and post the introduction event. Notably, the largest genetic differentiation was found in the intronic regions of the genes. In the NZ population, we also examined the association between polymorphisms in DRD4 and SERT and two highly repeatable behavioural traits: flight‐initiation distance and mating status (promiscuous females and cobreeding males). We found 38 significant associations (for different allele effect models) between the two behavioural traits and the studied genes. Further, 22 of the tested associations showed antagonistic allele effects for males and females. Our findings illustrate how introduction events and accompanying ecological changes could influence the genetic diversity of behaviour‐related genes.

Macroecology of parental care in arthropods: higher mortality risk leads to higher benefits of offspring protection in tropical climates.

The intensity of biotic interactions varies around the world, in such a way that mortality risk imposed by natural enemies is usually higher in the tropics. A major role of offspring attendance is protection against natural enemies, so the benefits of this behaviour should be higher in tropical regions. We tested this macroecological prediction with a meta‐regression of field experiments in which the mortality of guarded and unguarded broods was compared in arthropods. Mortality of unguarded broods was higher, and parental care was more beneficial, in warmer, less seasonal environments. Moreover, in these same environments, additional lines of defence further reduced offspring mortality, implying that offspring attendance alone is not enough to deter natural enemies in tropical regions. These results help to explain the high frequency of parental care among tropical species and how biotic interactions influence the occurrence of parental care over large geographic scales. Finally, our findings reveal that additional lines of defences – an oftentimes neglected component of parental care – have an important effect on the covariation between the benefits of parental care and the climate‐mediated mortality risk imposed by natural enemies.

Conflict and cooperation over sex: the consequences of social and genetic polyandry for reproductive success in dunnocks

Conflict and cooperation within and between the sexes are among the driving forces that lead to the evolution of mating systems. Among mating strategies, female genetic polyandry and male reproductive cooperation pose challenging evolutionary questions regarding the maintenance of systems where one sex suffers from reduced fitness. Here, we investigate the consequences of social and genetic polyandry for reproductive success of females and males in a population of the dunnock, Prunella modularis. We show that female multiple mating ameliorates the negative effects of inbreeding. We, however, found little evidence that females engage in extra-group (pair) mating with less related or more heterozygous males. Breeding in socially polyandrous groups reduced the amount of paternity lost to extra-group males, such that, on average, cobreeding and monogamous males fledged a similar number of young. Importantly, c. 30% of cobreeding male dyads were related, suggesting they could gain indirect fitness benefits. Taken together, cobreeding males achieve equivalent reproductive success to monogamous counterparts under most circumstances. Our study has revealed unexpected complexities in the variable mating system of dunnocks in New Zealand. Our results differ from the well-known Cambridge dunnock study and can help our understanding of the evolution and maintenance of various breeding systems in the animal kingdom.

Species-specific differences in relative eye size are related to patterns of edge avoidance in an Amazonian rainforest bird community

Eye size shows a large degree of variation among species, even after correcting for body size. In birds, relatively larger eyes have been linked to predation risk, capture of mobile prey, and nocturnal habits. Relatively larger eyes enhance visual acuity and also allow birds to forage and communicate in low-light situations. Complex habitats such as tropical rain forests provide a mosaic of diverse lighting conditions, including differences among forest strata and at different distances from the forest edge. We examined in an Amazonian forest bird community whether microhabitat occupancy (defined by edge avoidance and forest stratum) was a predictor of relative eye size. We found that relative eye size increased with edge avoidance, but did not differ according to forest stratum. Nevertheless, the relationship between edge avoidance and relative eye size showed a nonsignificant positive trend for species that inhabit lower forest strata. Our analysis shows that birds that avoid forest edges have larger eyes than those living in lighter parts. We expect that this adaptation may allow birds to increase their active daily period in dim areas of the forest. The pattern that we found raises the question of what factors may limit the evolution of large eyes.

Low genetic and morphological differentiation between an introduced population of dunnocks in New Zealand and an ancestral population in England

Species invasions and exotic species introductions can be considered as ‘unplanned experiments’, which help us to understand the evolution of organisms. In this study, we investigated whether an exotic bird species, the dunnock (Prunella modularis), has diverged genetically and morphologically from its native source population (Cambridge, England) after introduction into a new environment (Dunedin, South Island of New Zealand; exotic population). We used a set of microsatellite markers and three morphological traits to quantify the divergence between these two populations. We quantified neutral genotypic differentiation between the populations, and also used an individual-based Bayesian clustering method to assess genetic structure. We compared morphological divergence using univariate and principal components analyses. We found that individuals from the Dunedin population are genetically distinct from the Cambridge population, but levels of differentiation are very low. Overall within-population levels of genetic diversity are low compared to other bird species, and effective population sizes are small; indicating that the native population probably has a historically low level of genetic diversity, and that the introduced population retained most of that diversity after its introduction into New Zealand. We found little evidence of morphological divergence, and the evolutionary rate of change in these traits is below the average for other taxa. Our study adds support to the growing literature showing that invasive species maintain most of their initial genetic diversity after multiple founder events, even when population size is severely reduced. Moreover, our morphological data indicate slow evolutionary rates in species introduced to similar habitats.