Implementing code review in the scientific workflow: Insights from ecology and evolutionary biology.

Code review increases reliability and improves reproducibility of research. As such, code review is an inevitable step in software development and is common in fields such as computer science. However, despite its importance, code review is noticeably lacking in ecology and evolutionary biology. This is problematic as it facilitates the propagation of coding errors and a reduction in reproducibility and reliability of published results. To address this, we provide a detailed commentary on how to effectively review code, how to set up your project to enable this form of review and detail its possible implementation at several stages throughout the research process. This guide serves as a primer for code review, and adoption of the principles and advice here will go a long way in promoting more open, reliable, and transparent ecology and evolutionary biology.

Low availability of code in ecology: A call for urgent action.

Access to analytical code is essential for transparent and reproducible research. We review the state of code availability in ecology using a random sample of 346 nonmolecular articles published between 2015 and 2019 under mandatory or encouraged code-sharing policies. Our results call for urgent action to increase code availability: only 27% of eligible articles were accompanied by code. In contrast, data were available for 79% of eligible articles, highlighting that code availability is an important limiting factor for computational reproducibility in ecology. Although the percentage of ecological journals with mandatory or encouraged code-sharing policies has increased considerably, from 15% in 2015 to 75% in 2020, our results show that code-sharing policies are not adhered to by most authors. We hope these results will encourage journals, institutions, funding agencies, and researchers to address this alarming situation.

No evidence of immediate fitness benefits of within-season divorce in monogamous birds.

Individuals of socially monogamous species can correct for suboptimal partnerships via two secondary mating strategies: divorce and extra-pair mating, with the former potentially providing both genetic and social benefits. Divorcing between breeding seasons has been shown to be generally adaptive behaviour across monogamous birds. Interestingly, some pairs also divorce during the breeding season, when constraints on finding a new partner are stronger. Despite being important for a comprehensive understanding of the evolution of social monogamy, whether within-season divorce is adaptive and how it relates to extra-pair mating remains unknown. Here, we meta-analysed 90 effect sizes on within-season divorce and breeding success, extracted from 31 studies on 24 species. We found no evidence that within-season divorce is adaptive for breeding success. However, the large heterogeneity of effect sizes and strong phylogenetic signal suggest social and environmental factors-which have rarely been considered in empirical studies-may play an important role in explaining variation among populations and species. Furthermore, we found no evidence that within-season divorce and extra-pair mating are complementary strategies. We discuss our findings within the current evidence of the adaptiveness of secondary mating strategies and their interplay that ultimately shapes the evolution of social monogamy.

Towards open, reliable, and transparent ecology and evolutionary biology.

Unreliable research programmes waste funds, time, and even the lives of the organisms we seek to help and understand. Reducing this waste and increasing the value of scientific evidence require changing the actions of both individual researchers and the institutions they depend on for employment and promotion. While ecologists and evolutionary biologists have somewhat improved research transparency over the past decade (e.g. more data sharing), major obstacles remain. In this commentary, we lift our gaze to the horizon to imagine how researchers and institutions can clear the path towards more credible and effective research programmes.

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.

Familiarity breeds success: pairs that meet earlier experience increased breeding performance in a wild bird population.

In socially monogamous animals, including humans, pairs can meet and spend time together before they begin reproduction. However, the pre-breeding period has been challenging to study in natural populations, and thus remains largely unexplored. As such, our understanding of the benefits of mate familiarity is almost entirely limited to assessments of repeated breeding with a particular partner. Here, we used fine-scale tracking technology to gather 6 years of data on pre-breeding social associations of individually marked great tits in a wild population. We show that pairs which met earlier in the winter laid their eggs earlier in all years. Clutch size, number of hatched and fledged young, and hatching and fledging success were not influenced by parents' meeting time directly, but indirectly: earlier laying pairs had larger clutches (that also produce higher number of young), and higher hatching and fledging success. We did not detect a direct influence of the length of the initial pairing period on future mating decisions (stay with a partner or divorce). These findings suggest a selective advantage for a new pair to start associating earlier (or for individuals to mate with those they have known for longer). We call for more studies to explore the generality of fitness effects of pair familiarity prior to first breeding, and to elucidate the mechanisms underlying these effects.

Bats use social information within and across species.

In Focus: Lewanzik, D., Sundaramurthy, A. K., Goerlitz, H. R. (2019). Insectivorous bats integrate social information about species identity, conspecific activity and prey abundance to estimate cost-benefit ratio of interactions. Journal of Animal Ecology, 88, 1462-1473. Social interactions can generate social structures that shape the fate of individuals and populations. A key feature of social environments is the information produced by others. Whether actively shared or obtained via 'eavesdropping', individuals of many species use publically available information to guide their decision making in important ways. Lewanzik et al. (2019) explore social information use within and across several echolocating bat species. They experimentally manipulated the content of social information about prey abundance with playback experiments of echolocation calls. All species were found to use heterospecific and conspecific social information about conspecific activity levels and prey abundance. This is a rare experimental confirmation of social information use at a community level.

Live fast, don't die young: Survival-reproduction trade-offs in long-lived income breeders.

Trade-offs between survival and reproduction are at the core of life-history theory, and essential to understanding the evolution of reproductive tactics as well as population dynamics and stability. Factors influencing these trade-offs are multiple and often addressed in isolation. Further problems arise as reproductive states and survival in wild populations are estimated based on imperfect and potentially biased observation processes, which might lead to flawed conclusions. In this study, we aimed at elucidating trade-offs between current reproduction (both pregnancy and lactation), survival and future reproduction, including the specific costs of first reproduction, in long-lived, income breeding small mammals, an under-studied group. We developed a novel statistical framework that encapsulates the breeding life cycle of females, and accounts for incomplete information on female pregnancy and lactation and imperfect and biased recapture rates. We applied this framework to longitudinal data on two sympatric, closely related bat species (Myotis daubentonii and M. nattereri). We revealed the existence of several, to our knowledge previously unknown, trends in survival and breeding of these closely related, sympatric species and detected remarkable differences in their age and costs of first reproduction, as well as their survival-reproduction trade-offs. Our results indicate that species with this type of life history exhibit a mixture of patterns expected for long-lived and short-lived animals, and between income and capital breeders. Thus, we call for more studies to be conducted in similar study systems, increasing our ability to fully understand the evolutionary origin and fitness effects of trade-offs and senescence.

Quantitative analysis of the dose-response of white spot syndrome virus in shrimp.

White spot syndrome virus (WSSV) is an important cause of mortality and economic losses in shrimp farming. Although WSSV-induced mortality is virus dose dependent and WSSV infection does not necessarily lead to mortality, the relationships between virus-particle dose, infection and mortality have not been analysed quantitatively. Here, we explored WSSV dose-response by a combination of experiments, modelling and meta-analysis. We performed dose-response experiments in Penaeus vannamei postlarvae, recorded host mortality and detected WSSV infection. When we fitted infection models to these data, two models-differing in whether they incorporated heterogeneous host susceptibility to the virus or not-were supported for two independent experiments. To determine the generality of these results, we reanalysed published data sets and then performed a meta-analysis. We found that WSSV dose-response kinetics is indeed variable over experiments. We could not clearly identify which specific infection model has the most support by meta-analysis, but we argue that these results also are most concordant with a model incorporating varying levels of heterogeneous host susceptibility to WSSV. We have identified suitable models for analysing WSSV dose-response, which can elucidate the most basic virus-host interactions and help to avoid underestimating WSSV infection at low virus doses.

Carry-over effects of the social environment on future divorce probability in a wild bird population.

Initial mate choice and re-mating strategies (infidelity and divorce) influence individual fitness. Both of these should be influenced by the social environment, which determines the number and availability of potential partners. While most studies looking at this relationship take a population-level approach, individual-level responses to variation in the social environment remain largely unstudied. Here, we explore carry-over effects on future mating decisions of the social environment in which the initial mating decision occurred. Using detailed data on the winter social networks of great tits, we tested whether the probability of subsequent divorce, a year later, could be predicted by measures of the social environment at the time of pairing. We found that males that had a lower proportion of female associates, and whose partner ranked lower among these, as well as inexperienced breeders, were more likely to divorce after breeding. We found no evidence that a female's social environment influenced the probability of divorce. Our findings highlight the importance of the social environment that individuals experience during initial pair formation on later pairing outcomes, and demonstrate that such effects can be delayed. Exploring these extended effects of the social environment can yield valuable insights into processes and selective pressures acting upon the mating strategies that individuals adopt.

Supporting study registration to reduce research waste.

An estimated 82-89% of ecological research and 85% of medical research has limited or no value to the end user because of various inefficiencies. We argue that registration and registered reports can enhance the quality and impact of ecological research. Drawing on evidence from other fields, chiefly medicine, we support our claim that registration can reduce research waste. However, increasing registration rates, quality and impact will be very slow without coordinated effort of funders, publishers and research institutions. We therefore call on them to facilitate the adoption of registration by providing adequate support. We outline several aspects to be considered when designing a registration system that would best serve the field of ecology. To further inform the development of such a system, we call for more research to identify the causes of low registration rates in ecology. We suggest short- and long-term actions to bolster registration and reduce research waste.

The effect of the COVID-19 pandemic on the gender gap in research productivity within academia.

Using measures of research productivity to assess academic performance puts women at a disadvantage because gender roles and unconscious biases, operating both at home and in academia, can affect research productivity. The impact of the COVID-19 pandemic on research productivity has been the subject of a number of studies, including studies based on surveys and studies based on numbers of articles submitted to and/or published in journals. Here, we combine the results of 55 studies that compared the impact of the pandemic on the research productivity of men and women; 17 of the studies were based on surveys, 38 were based on article counts, and the total number of effect sizes was 130. We find that the gender gap in research productivity increased during the COVID-19 pandemic, with the largest changes occurring in the social sciences and medicine, and the changes in the biological sciences and TEMCP (technology, engineering, mathematics, chemistry and physics) being much smaller.

Quantifying research waste in ecology.

Research inefficiencies can generate huge waste: evidence from biomedical research has shown that most research is avoidably wasted and steps have been taken to tackle this costly problem. Although other scientific fields could also benefit from identifying and quantifying waste and acting to reduce it, no other estimates of research waste are available. Given that ecological issues interweave most of the United Nations Sustainable Development Goals, we argue that tackling research waste in ecology should be prioritized. Our study leads the way. We estimate components of waste in ecological research based on a literature review and a meta-analysis. Shockingly, our results suggest only 11-18% of conducted ecological research reaches its full informative value. All actors within the research system-including academic institutions, policymakers, funders and publishers-have a duty towards science, the environment, study organisms and the public, to urgently act and reduce this considerable yet preventable loss. We discuss potential ways forward and call for two major actions: (1) further research into waste in ecology (and beyond); (2) focused development and implementation of solutions to reduce unused potential of ecological research.

Environmental coupling of heritability and selection is rare and of minor evolutionary significance in wild populations.

Predicting the rate of adaptation to environmental change in wild populations is important for understanding evolutionary change. However, predictions may be unreliable if the two key variables affecting the rate of evolutionary change-heritability and selection-are both affected by the same environmental variable. To determine how general such an environmentally induced coupling of heritability and selection is, and how this may influence the rate of adaptation, we made use of freely accessible, open data on pedigreed wild populations to answer this question at the broadest possible scale. Using 16 populations from 10 vertebrate species, which provided data on 50 traits (relating to body mass, morphology, physiology, behaviour and life history), we found evidence for an environmentally induced relationship between heritability and selection in only 6 cases, with weak evidence that this resulted in an increase or decrease in the expected selection response. We conclude that such a coupling of heritability and selection is unlikely to strongly affect evolutionary change, even though both heritability and selection are commonly postulated to be dependent on the environment.

Navigating the unfolding open data landscape in ecology and evolution.

Open access to data is revolutionizing the sciences. To allow ecologists and evolutionary biologists to confidently find and use the existing data, we provide an overview of the landscape of online data infrastructures, and highlight the key points to consider when using open data. We introduce an online collaborative platform to keep a community-driven, updated list of the best sources that enable search for data in one interface. In doing so, our aim is to lower the barrier to accessing open data, and encourage its use by researchers hoping to increase the scope, reliability and value of their findings.

Personality shapes pair bonding in a wild bird social system.

Mated pair bonds are integral to many animal societies, yet how individual variation in behaviour influences their formation remains largely unknown. In a population of wild great tits (Parus major), we show that personality shapes pair bonding: proactive males formed stronger pre-breeding pair bonds by meeting their future partners sooner and increasing their relationship strength at a faster rate. As a result, proactive males sampled fewer potential mates. Thus, personality may have important implications for social relationship dynamics and emergent social structure.

Trading up: the fitness consequences of divorce in monogamous birds.

Social and genetic mating systems play an important role in natural and sexual selection, as well as in the dynamics of populations. In socially monogamous species different genetic mating patterns appear when individuals mate outside the breeding pair within a breeding season (extra-pair mating) or when they change partners between two breeding seasons (widowing or divorce). Divorce can be defined as having occurred when two previously paired individuals are alive during the next breeding season and at least one of them has re-mated with a new partner. In socially monogamous birds divorce is widespread, but it is not clear whether it is a behavioural adaptation to improve the quality of a mating decision or whether, alternatively, it results as a non-selected consequence of other processes: existing studies suggest a heterogeneous set of results with respect to this central question. This heterogeneity could result from a number of factors, ranging from the methodological approaches used, to population- or species-specific characters. In this review we use phylogenetic meta-analyses to assess the evidence that divorce is adaptive (in terms of breeding success) across 64 species of socially monogamous birds. Second, we explore biological and methodological reasons for the heterogeneity in the results of previous studies. Results of our analyses supported the hypothesis that divorce is, in general, an adaptive behavioural strategy as: (1) divorce is triggered by relatively low breeding success; (2) there is a positive change in breeding success as a result of divorce. More specifically, while controlling for methodological moderators, we show that: (i) earlier stages of breeding are better predictors of divorce than later stages (r = 0.231; 95% CI: 0.061-0.391 for clutch size; similar for laying date); (ii) females benefited from divorce more than males in terms of increasing breeding success between successive breeding attempts, with different stages of the breeding cycle improving at different rates (e.g. r = 0.637; 95% CI: 0.328-0.817 for brood-level measures). We show that the effect size was dependent on the methodological approach used across studies and argue that research on the adaptive nature of divorce should be cautious when designing the study and interpreting the results. Altogether, by providing strong evidence that divorce is an adaptive strategy across monogamous birds, the results of our analysis provide a firm ground for further exploration of external covariates of divorce (e.g. demographic factors) and the mechanisms underlying the differences in the effect sizes of the proximal fitness causes and consequences of divorce.

The role of social and ecological processes in structuring animal populations: a case study from automated tracking of wild birds.

Both social and ecological factors influence population process and structure, with resultant consequences for phenotypic selection on individuals. Understanding the scale and relative contribution of these two factors is thus a central aim in evolutionary ecology. In this study, we develop a framework using null models to identify the social and spatial patterns that contribute to phenotypic structure in a wild population of songbirds. We used automated technologies to track 1053 individuals that formed 73 737 groups from which we inferred a social network. Our framework identified that both social and spatial drivers contributed to assortment in the network. In particular, groups had a more even sex ratio than expected and exhibited a consistent age structure that suggested local association preferences, such as preferential attachment or avoidance. By contrast, recent immigrants were spatially partitioned from locally born individuals, suggesting differential dispersal strategies by phenotype. Our results highlight how different scales of social decision-making, ranging from post-natal dispersal settlement to fission-fusion dynamics, can interact to drive phenotypic structure in animal populations.