Best practices for genetic and genomic data archiving.

Genetic and genomic data are collected for a vast array of scientific and applied purposes. Despite mandates for public archiving, data are typically used only by the generating authors. The reuse of genetic and genomic datasets remains uncommon because it is difficult, if not impossible, due to non-standard archiving practices and lack of contextual metadata. But as the new field of macrogenetics is demonstrating, if genetic data and their metadata were more accessible and FAIR (findable, accessible, interoperable and reusable) compliant, they could be reused for many additional purposes. We discuss the main challenges with existing genetic and genomic data archives, and suggest best practices for archiving genetic and genomic data. Recognizing that this is a longstanding issue due to little formal data management training within the fields of ecology and evolution, we highlight steps that research institutions and publishers could take to improve data archiving.

Advancing Inclusive Biodiversity Research: Strategies for Equitable Practices and Collective Impact / Promovendo a Pesquisa Inclusiva em Biodiversidade: Estratégias para Práticas Equitativas e Impacto Coletivo

Biodiversity research is essential for addressing the global biodiversity crisis, necessitating diverse participation and perspectives. However, the field currently faces a significant inclusivity problem as local expertise from biodiversity-rich but economically disadvantaged regions is often underrepresented. The underrepresentation of local experts is driven by four main challenges: linguistic bias, undervalued contributions, parachute science practices, and capacity constraints. While fragmented solutions exist, a unified multi-stakeholder approach is necessary to address these interconnected and systemic issues. Here, we introduce a holistic framework of collective responsibility, integrating tailored strategies that embrace diversity and dismantle systemic barriers for equitable collaboration. This framework delineates the diverse actors and practices required for promoting inclusivity in biodiversity research, assigning clear responsibilities to researchers, publishers, institutions, and funding bodies. Strategies for researchers include cultivating self-awareness, expanding literature searches, fostering partnerships with local experts, and promoting knowledge exchange. For institutions, we recommend establishing specialized liaison roles, implementing equitable policies, allocating resources for diversity initiatives, and enhancing support for international researchers. Publishers can facilitate multilingual dissemination, remove financial barriers, establish inclusivity standards, and ensure equitable representation in peer review. Funders should remove systemic barriers, strengthen research networks, and prioritize equitable resource allocation. Implementing these stakeholder-specific strategies can help dismantle deep-rooted biases and structural inequities in biodiversity research, catalyzing a shift towards a more inclusive and representative model that amplifies diverse perspectives and maximizes collective knowledge for effective global conservation.

A pesquisa em biodiversidade é essencial para enfrentar a crise global de biodiversidade, exigindo perspectivas diversificadas. No entanto, este campo do conhecimento enfrenta um significativo problema de inclusão, uma vez que os conhecimentos ecológicos produzidos em áreas ricas em biodiversidade, mas economicamente desfavorecidas, são frequentemente sub-representados. Esta sub-representação é impulsionada por quatro desafios principais: viés linguístico, contribuições científicas subvalorizadas, colaborações baseadas em práticas colonialistas (parachute science) e lacunas na capacitação e no acesso a dados. Embora soluções fragmentadas existam, uma abordagem multilateral unificada é necessária para abordar estas questões sistêmicas. Aqui, introduzimos uma abordagem holística de responsabilidade coletiva, integrando estratégias personalizadas que abraçam a diversidade e desmantelam barreiras sistêmicas para uma colaboração equitativa. Esta abordagem delineia os diversos atores e práticas necessárias para promover a inclusão na pesquisa sobre biodiversidade, atribuindo responsabilidades claras a pesquisadores, editoras, instituições e órgãos de fomento. As estratégias para os investigadores incluem o cultivo da autoconsciência, a expansão das pesquisas bibliográficas, o fomento de parcerias com especialistas locais e a promoção do intercâmbio de conhecimentos. Para as instituições, recomendamos o estabelecimento de funções de intermediação especializadas, a implementação de políticas equitativas, a alocação de recursos para iniciativas de diversidade e o reforço do apoio a pesquisadores internacionais. As editoras podem facilitar a divulgação multilíngue, eliminar barreiras financeiras, estabelecer normas de inclusão e assegurar uma representação equitativa na avaliação pelos pares. Os financiadores devem eliminar barreiras sistêmicas, fortalecer redes de pesquisa e dar prioridade à distribuição equitativa de recursos. A implementação dessas estratégias específicas para as partes interessadas pode ajudar a desmantelar vieses profundamente enraizados e desigualdades estruturais na pesquisa de biodiversidade, catalisando uma mudança para um modelo mais inclusivo e representativo que amplifica perspectivas diversas e maximiza o conhecimento coletivo para uma eficaz conservação da biodiversidade global.

Advancing Inclusive Biodiversity Research: Strategies for Equitable Practices and Collective Impact / Promoción de la investigación inclusiva sobre la biodiversidad: estrategias para prácticas equitativas e impacto colectivo

Biodiversity research is essential for addressing the global biodiversity crisis, necessitating diverse participation and perspectives. However, the field currently faces a significant inclusivity problem as local expertise from biodiversity-rich but economically disadvantaged regions is often underrepresented. The underrepresentation of local experts is driven by four main challenges: linguistic bias, undervalued contributions, parachute science practices, and capacity constraints. While fragmented solutions exist, a unified multi-stakeholder approach is necessary to address these interconnected and systemic issues. Here, we introduce a holistic framework of collective responsibility, integrating tailored strategies that embrace diversity and dismantle systemic barriers for equitable collaboration. This framework delineates the diverse actors and practices required for promoting inclusivity in biodiversity research, assigning clear responsibilities to researchers, publishers, institutions, and funding bodies. Strategies for researchers include cultivating self-awareness, expanding literature searches, fostering partnerships with local experts, and promoting knowledge exchange. For institutions, we recommend establishing specialized liaison roles, implementing equitable policies, allocating resources for diversity initiatives, and enhancing support for international researchers. Publishers can facilitate multilingual dissemination, remove financial barriers, establish inclusivity standards, and ensure equitable representation in peer review. Funders should remove systemic barriers, strengthen research networks, and prioritize equitable resource allocation. Implementing these stakeholder-specific strategies can help dismantle deep-rooted biases and structural inequities in biodiversity research, catalyzing a shift towards a more inclusive and representative model that amplifies diverse perspectives and maximizes collective knowledge for effective global conservation.

La investigación sobre la biodiversidad es esencial para hacer frente a la crisis mundial de la biodiversidad, lo cual requiere una participación y perspectivas diversas. Sin embargo, el estudio de la biodiversidad se enfrenta actualmente a un importante problema de inclusión, ya que los conocimientos locales de regiones altamente biodiversas, aunque económicamente desfavorecidas, suelen tener menor representación. La escasa representación de los expertos locales se debe a cuatro retos principales: el sesgo lingüístico, la subestimación de contribuciones, las prácticas científicas de paracaídas y las limitaciones de capacidad. Si bien existen soluciones fragmentadas, es necesario un enfoque unificado de múltiples partes interesadas para abordar estos problemas interconectados y sistémicos. Aquí, presentamos un marco holístico de responsabilidad colectiva, integrando estrategias personalizadas que abrazan la diversidad y desmantelan las barreras sistémicas para una colaboración equitativa. Este marco delinea los diversos actores y prácticas necesarias para promover la inclusión en la investigación sobre biodiversidad, asignando responsabilidades claras a investigadores, editores, instituciones y organismos de financiación. Las estrategias para los investigadores incluyen cultivar la autoconciencia, la ampliación de las búsquedas bibliográficas, el fomento de asociaciones con expertos locales y la promoción del intercambio de conocimientos. En el caso de las instituciones, recomendamos establecer funciones de colaboración especializadas, implementar políticas equitativas, asignar recursos para iniciativas de diversidad y mejorar el apoyo a los investigadores internacionales. Los editores pueden facilitar la difusión multilingüe, eliminar las barreras financieras, establecer normas de inclusión y garantizar una representación equitativa en la revisión por pares. Los financiadores deben eliminar las barreras sistémicas, fortalecer las redes de investigación y priorizar la asignación equitativa de recursos. La implementación de estas estrategias específicas para las partes interesadas puede ayudar a desmantelar los sesgos profundamente arraigados y las desigualdades estructurales en la investigación sobre biodiversidad, catalizando un cambio hacia un modelo más inclusivo y representativo que amplifique las diversas perspectivas y maximice el conocimiento colectivo para una conservación global efectiva.

Investigating the Relationship Between Body Shape and Life History Traits in Toothed Whales: Can Body Shape Predict Fast-Slow Life Histories?

A widespread pattern in vertebrate life-history evolution is for species to evolve towards either fast or slow life histories; however, the underlying causes of this pattern remain unclear. Toothed whales (Odontoceti) are a diverse group with a range of body sizes and life histories, making them an ideal model to investigate potential drivers of this dichotomy. Using ancestral reconstruction, we identified that certain groups of odontocetes evolved more-streamlined, presumably faster, body shapes around the same time that killer whales (Orcinus orca) evolved into whale predators approximately 1 Mya during the Pleistocene. This suggests that the evolution of a streamlined body shape may have been an adaptation to escape killer whale predation, leading to longer life-history events. To test this hypothesis, we performed a cluster analysis of odontocete whales and confirmed the dual pattern of life-history traits, with one group referred to as 'reproducers' characterized by early age of maturity, short gestation, short interbirth interval, and short lifespan, and the other group referred to as 'bet-hedgers' exhibiting the opposite pattern. However, we found that life history grouping was relatively unrelated to whale shape (i.e., more streamlined or less streamlined). Therefore, we incorporated principal component results into mixed effects models, and the model results indicated that body shape was positively related to neonate length (a measure of investment in progeny), but not significantly related to the temporal life-history traits. Thus, whale body shape is not a sufficient explanation for the evolution of fast-slow life histories in odontocete whales. Supplementary Information: The online version contains supplementary material available at 10.1007/s11692-023-09605-4.

Conservation macrogenetics: harnessing genetic data to meet conservation commitments.

Genetic biodiversity is rapidly gaining attention in global conservation policy. However, for almost all species, conservation relevant, population-level genetic data are lacking, limiting the extent to which genetic diversity can be used for conservation policy and decision-making. Macrogenetics is an emerging discipline that explores the patterns and processes underlying population genetic composition at broad taxonomic and spatial scales by aggregating and reanalyzing thousands of published genetic datasets. Here we argue that focusing macrogenetic tools on conservation needs, or conservation macrogenetics, will enhance decision-making for conservation practice and fill key data gaps for global policy. Conservation macrogenetics provides an empirical basis for better understanding the complexity and resilience of biological systems and, thus, how anthropogenic drivers and policy decisions affect biodiversity.

The evolution of plasticity at geographic range edges.

Phenotypic plasticity enables rapid responses to environmental change, and could facilitate range shifts in response to climate change. What drives the evolution of plasticity at range edges, and the capacity of range-edge individuals to be plastic, remain unclear. Here, we propose that accurately predicting when plasticity itself evolves or mediates adaptive evolution at expanding range edges requires integrating knowledge on the demography and evolution of edge populations. Our synthesis shows that: (i) the demography of edge populations can amplify or attenuate responses to selection for plasticity through diverse pathways, and (ii) demographic effects on plasticity are modified by the stability of range edges. Our spatially explicit synthesis for plasticity has the potential to improve predictions for range shifts with climate change.

Survey of Toxoplasma gondii in Urban and Rural Squirrels (Sciuridae) in Manitoba, Canada.

The coccidian parasite Toxoplasma gondii is found worldwide infecting warm-blooded vertebrates. Felids are the definitive hosts; other species act as intermediate hosts. Squirrels (Sciuridae) generally have high population densities in cities and forage and cache food on the ground, where they may come into contact with T. gondii oocysts or be preyed upon by cats and other carnivores. This environment might make squirrels important intermediate hosts of T. gondii in cities, and infection rates could indicate environmental levels of oocysts in soil. We investigated whether urban squirrels would be more exposed to T. gondii infection than rural squirrels with samples collected from American red squirrels (Tamiasciurus hudsonicus), eastern grey squirrels (Sciurus carolinensis), northern flying squirrels (Glaucomys sabrinus), and least chipmunks (Tamias minimus) in and around Winnipeg, Manitoba, Canada. We tested 230 tissue samples from 46 squirrels for T. gondii DNA by quantitative PCR and 13 serum samples from grey squirrels for T. gondii antibodies by competitive ELISA. We found no evidence of infection in any squirrel, indicating that squirrels are probably not important intermediate hosts of T. gondii in cities and that consumption of oocysts in the soil in general may not be an important contributor to transmission in colder environments.

Genetic diversity and IUCN Red List status.

The International Union for Conservation of Nature (IUCN) Red List is an important and widely used tool for conservation assessment. The IUCN uses information about a species' range, population size, habitat quality and fragmentation levels, and trends in abundance to assess extinction risk. Genetic diversity is not considered, although it affects extinction risk. Declining populations are more strongly affected by genetic drift and higher rates of inbreeding, which can reduce the efficiency of selection, lead to fitness declines, and hinder species' capacities to adapt to environmental change. Given the importance of conserving genetic diversity, attempts have been made to find relationships between red-list status and genetic diversity. Yet, there is still no consensus on whether genetic diversity is captured by the current IUCN Red List categories in a way that is informative for conservation. To assess the predictive power of correlations between genetic diversity and IUCN Red List status in vertebrates, we synthesized previous work and reanalyzed data sets based on 3 types of genetic data: mitochondrial DNA, microsatellites, and whole genomes. Consistent with previous work, species with higher extinction risk status tended to have lower genetic diversity for all marker types, but these relationships were weak and varied across taxa. Regardless of marker type, genetic diversity did not accurately identify threatened species for any taxonomic group. Our results indicate that red-list status is not a useful metric for informing species-specific decisions about the protection of genetic diversity and that genetic data cannot be used to identify threat status in the absence of demographic data. Thus, there is a need to develop and assess metrics specifically designed to assess genetic diversity and inform conservation policy, including policies recently adopted by the UN's Convention on Biological Diversity Kunming-Montreal Global Biodiversity Framework.

La diversidad genética y los estados de la Lista Roja de la UICN Resumen La Lista Roja de la Unión Internacional para la Conservación de la Naturaleza (UICN) es una importante herramienta de uso extendido para evaluar la conservación. La UICN utiliza datos sobre la distribución y tamaño poblacional de una especie, la calidad y niveles de fragmentación de su hábitat y sus tendencias de abundancia para valorar su riesgo de extinción, A pesar de que la diversidad genética afecta al riesgo de extinción, la UICN no la considera. La deriva génica y las tasas altas de endogamia afectan con mayor fuerza a las poblaciones en declinación, lo que puede reducir la eficiencia de la selección, derivar en la disminución de la aptitud y dificultar la capacidad de una especie de adaptarse ante el cambio ambiental. Se ha intentado encontrar la relación entre la diversidad genética y el estado en las listas rojas ya que su conservación es muy importante. Aun con lo anterior, no hay un consenso actual sobre si la diversidad genética está capturada en las categorías vigentes de la Lista Roja de la UICN de manera que sea informativa para la conservación. Para poder evaluar el poder predictivo de la correlación entre la diversidad genética y el estado en la Lista Roja de los vertebrados, sintetizamos trabajos previos y analizamos de nuevo los conjuntos de datos con base en tres tipos de información genética: ADN mitocondrial, microsatélites y genomas completos. Las especies con un estado de riesgo de extinción más alto fueron propensas a una diversidad genética más baja para todos los tipos de marcadores, aunque estas relaciones fueron débiles y variaron entre los taxones, lo cual es coherente con trabajos anteriores. Sin importar el tipo de marcador, la diversidad genética no fue un identificador certero de las especies amenazadas en ninguno de los grupos taxonómicos. Nuestros resultados indican que el estado de lista roja no es una medida útil para guiar las decisiones específicas por especie en relación con la protección de la diversidad genética. También indican que los datos genéticos no pueden usarse para identificar el estado de amenaza si no se tienen los datos demográficos. Por lo tanto, es necesario desarrollar y evaluar las medidas diseñadas específicamente para valorar la diversidad genética e informar las políticas de conservación, incluidas las que adoptó recientemente la ONU en el Convenio del Marco Mundial Kunming-Montreal de la Diversidad Biológica.

Systemic racism alters wildlife genetic diversity.

In the United States, systemic racism has had lasting effects on the structure of cities, specifically due to government-mandated redlining policies that produced racially segregated neighborhoods that persist today. However, it is not known whether varying habitat structures and natural resource availability associated with racial segregation affect the demographics and evolution of urban wildlife populations. To address this question, we repurposed and reanalyzed publicly archived nuclear genetic data from 7,698 individuals spanning 39 terrestrial vertebrate species sampled in 268 urban locations throughout the United States. We found generally consistent patterns of reduced genetic diversity and decreased connectivity in neighborhoods with fewer White residents, likely because of environmental differences across these neighborhoods. The strength of relationships between the racial composition of neighborhoods, genetic diversity, and differentiation tended to be weak relative to other factors affecting genetic diversity, possibly in part due to the recency of environmental pressures on urban wildlife populations. However, the consistency of the direction of effects across disparate taxa suggest that systemic racism alters the demography of urban wildlife populations in ways that generally limit population sizes and negatively affect their chances of persistence. Our results thus support the idea that limited capacity to support large, well-connected wildlife populations reduces access to nature and builds on existing environmental inequities shouldered by predominantly non-White neighborhoods.

Population demography maintains biogeographic boundaries.

Global biodiversity is organised into biogeographic regions that comprise distinct biotas. The contemporary factors maintaining differences in species composition between regions are poorly understood. Given evidence that populations with sufficient genetic variation can adapt to fill new habitats, it is surprising that more homogenisation of species assemblages across regions has not occurred. Theory suggests that expansion across biogeographic regions could be limited by reduced adaptive capacity due to demographic variation along environmental gradients, but this possibility has not been empirically explored. Using three independently curated data sets describing continental patterns of mammalian demography and population genetics, we show that populations near biogeographic boundaries have lower effective population sizes and genetic diversity, and are more genetically differentiated. These patterns are consistent with reduced adaptive capacity in areas where one biogeographic region transitions into the next. That these patterns are replicated across mammals suggests they are stable and generalisable in their contribution to long-term limits on biodiversity homogenisation. Understanding the contemporary processes that maintain compositional differences among regional biotas is crucial for our understanding of the current and future organisation of global biodiversity.

Genetic and species-level biodiversity patterns are linked by demography and ecological opportunity.

The processes that give rise to species richness gradients are not well understood, but may be linked to resource-based limits on the number of species a region can support. Ecological limits placed on regional species richness should also affect population demography, suggesting that these processes could also generate genetic diversity gradients. If true, we might better understand how broad-scale biodiversity patterns are formed by identifying the common causes of genetic diversity and species richness. We develop a hypothetical framework based on the consequences of regional variation in ecological limits set by resource availability and heterogeneity to simultaneously explain spatial patterns of species richness and neutral genetic diversity. Repurposing raw genotypic data spanning 38 mammal species sampled across 801 sites in North America, we show that estimates of genome-wide genetic diversity and species richness share spatial structure. Notably, species richness hotspots tend to harbor lower levels of within-species genetic variation. A structural equation model encompassing eco-evolutionary processes related to resource availability, habitat heterogeneity, and contemporary human disturbance supports the spatial patterns we detect. These results suggest broad-scale patterns of species richness and genetic diversity could both partly be caused by intraspecific demographic and evolutionary processes acting simultaneously across species.

Opportunities and challenges of macrogenetic studies.

The rapidly emerging field of macrogenetics focuses on analysing publicly accessible genetic datasets from thousands of species to explore large-scale patterns and predictors of intraspecific genetic variation. Facilitated by advances in evolutionary biology, technology, data infrastructure, statistics and open science, macrogenetics addresses core evolutionary hypotheses (such as disentangling environmental and life-history effects on genetic variation) with a global focus. Yet, there are important, often overlooked, limitations to this approach and best practices need to be considered and adopted if macrogenetics is to continue its exciting trajectory and reach its full potential in fields such as biodiversity monitoring and conservation. Here, we review the history of this rapidly growing field, highlight knowledge gaps and future directions, and provide guidelines for further research.

The population genetics of urban and rural amphibians in North America.

Human land transformation is one of the leading causes of vertebrate population declines. These declines are thought to be partly due to decreased connectivity and habitat loss reducing animal population sizes in disturbed habitats. With time, this can lead to declines in effective population size and genetic diversity which restrict the ability of wildlife to efficiently cope with environmental change through genetic adaptation. However, it is not well understood whether these effects generally hold across taxa. We address this question by repurposing and synthesizing raw microsatellite data from online repositories for 19 amphibian species sampled at 554 georeferenced sites in North America. For each site, we estimated gene diversity, allelic richness, effective population size, and population differentiation. Using binary urban-rural census designations, and continuous measures of human population density, the Human Footprint Index, and impervious surface cover, we tested for generalizable effects of human land use on amphibian genetic diversity. We found minimal evidence, either positive or negative, for relationships between genetic metrics and urbanization. Together with previous work on focal species that also found varying effects of urbanization on genetic composition, it seems likely that the consequences of urbanization are not easily generalizable within or across amphibian species. Questions about the genetic consequences of urbanization for amphibians should be addressed on a case-by-case basis. This contrasts with general negative effects of urbanization in mammals and consistent, but species-specific, positive and negative effects in birds.

Genomic evidence for parallel adaptation to cities.

Urban evolutionary biology is the study of rapid evolutionary change in response to humans and our uses of land to support city dwellers. Because cities are relatively modern additions to the natural world, research on urban evolution tends to focus on microevolutionary change that has happened across a few to many hundreds of generations. These questions still fall under the broad purview of evolutionary ecology. However, the severity, rapidity and replication of environmental changes that drive evolution in this context make it worthy of specific attention. Urban evolution provides the opportunity to study the earliest stages of evolution in a context that is scientifically interesting and societally important. The newness of urban populations and their proximity to natural populations also creates challenges when trying to detect population genetic change. In a From the Cover article in this issue of Molecular Ecology, Mueller et al. use whole genome resequencing data to address some of these challenges while exploring genetic changes associated with urbanization in three replicate urban-rural burrowing owl (Athene cunicularia) populations. Combining multiple approaches across these sample sites Mueller et al. find evidence for selection on genes whose function is related to synapses, neuron projections, brain connectivity and cognitive function in general. That selection was parallel suggests that phenotypes related to brain processes were probably particularly important for urban adaptation.

A New Framework for Urban Ecology: An Integration of Proximate and Ultimate Responses to Anthropogenic Change.

As urban areas continue to grow, understanding how species respond and adapt to urban habitats is becoming increasingly important. Knowledge of the mechanisms behind observed phenotypic changes of urban-dwelling animals will enable us to better evaluate the impact of urbanization on current and future generations of wildlife and predict how animals respond to novel environments. Recently, urban ecology has emerged not only as a means of understanding organismal adaptation but also as a framework for exploring mechanisms mediating evolutionary phenomena. Here, we have identified four important research topics that will advance the field of urban ecology and shed light on the proximate and ultimate causes of the phenotypic differences commonly seen among species and populations that vary in their responses to urbanization. First, we address the ecological and socio-economic factors that characterize cities, how they might interact with each other, and how they affect urban species. Second, we ask which are the proximate mechanisms underlying the emergence over time of novel traits in urban organisms, focusing on developmental effects. Third, we emphasize the importance of understanding the ultimate causations that link phenotypic shifts to function. This question highlights the need to quantify the strength and direction of selection that urban individuals are exposed to, and whether the phenotypic shifts associated with life in the city are adaptive. Lastly, we stress the need to translate how individual-level responses scale up to population dynamics. Understanding the mechanistic underpinnings of variation among populations and species in their responses to urbanization will unravel species resilience to environmental perturbation, which will facilitate predictive models for sustainability and development of green cities that maintain or even increase urban biodiversity and wildlife health and wellbeing.

Digest: Local adaptation at close quarters.

Although the theory of how gene flow and genetic drift interact with local adaptation is well understood, few empirical studies have examined this process. Hämälä et al. (2018) present evidence that adaptive divergence between populations of Arabidopsis lyrata can persist in the face of relatively high levels of gene flow and drift. Maintaining divergence despite gene flow and drift has important implications for understanding adaptive responses of populations in response to human-driven environmental change.