The dynamic adaptive landscape of cetacean body size.

Adaptive landscapes are central to evolutionary theory, forming a conceptual bridge between micro- and macroevolution.1,2,3,4 Evolution by natural selection across an adaptive landscape should drive lineages toward fitness peaks, shaping the distribution of phenotypic variation within and among clades over evolutionary timescales.5 The location and breadth of these peaks in phenotypic space can also evolve,4 but whether phylogenetic comparative methods can detect such patterns has largely remained unexplored.6 Here, we characterize the global and local adaptive landscape for total body length in cetaceans (whales, dolphins, and relatives), a trait that spans an order of magnitude, across their ∼53-million-year evolutionary history. Using phylogenetic comparative methods, we analyze shifts in long-term mean body length7 and directional changes in average trait values8 for 345 living and fossil cetacean taxa. Remarkably, we find that the global macroevolutionary adaptive landscape of cetacean body length is relatively flat, with very few peak shifts occurring after cetaceans entered the oceans. Local peaks are more numerous and manifest as trends along branches linked to specific adaptations. These results contrast with previous studies using only extant taxa,9 highlighting the vital role of fossil data for understanding macroevolution.10,11,12 Our results indicate that adaptive peaks are dynamic and are associated with subzones of local adaptations, creating moving targets for species adaptation. In addition, we identify limits in our ability to detect some evolutionary patterns and processes and suggest that multiple approaches are required to characterize complex hierarchical patterns of adaptation in deep time.

The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis.

Approximately 25% of mammals are currently threatened with extinction, a risk that is amplified under climate change. Species persistence under climate change is determined by the combined effects of climatic factors on multiple demographic rates (survival, development and reproduction), and hence, population dynamics. Thus, to quantify which species and regions on Earth are most vulnerable to climate-driven extinction, a global understanding of how different demographic rates respond to climate is urgently needed. Here, we perform a systematic review of literature on demographic responses to climate, focusing on terrestrial mammals, for which extensive demographic data are available. To assess the full spectrum of responses, we synthesize information from studies that quantitatively link climate to multiple demographic rates. We find only 106 such studies, corresponding to 87 mammal species. These 87 species constitute <1% of all terrestrial mammals. Our synthesis reveals a strong mismatch between the locations of demographic studies and the regions and taxa currently recognized as most vulnerable to climate change. Surprisingly, for most mammals and regions sensitive to climate change, holistic demographic responses to climate remain unknown. At the same time, we reveal that filling this knowledge gap is critical as the effects of climate change will operate via complex demographic mechanisms: a vast majority of mammal populations display projected increases in some demographic rates but declines in others, often depending on the specific environmental context, complicating simple projections of population fates. Assessments of population viability under climate change are in critical need to gather data that account for multiple demographic responses, and coordinated actions to assess demography holistically should be prioritized for mammals and other taxa.

Bridging gaps in demographic analysis with phylogenetic imputation.

Phylogenetically informed imputation methods have rarely been applied to estimate missing values in demographic data but may be a powerful tool for reconstructing vital rates of survival, maturation, and fecundity for species of conservation concern. Imputed vital rates could be used to parameterize demographic models to explore how populations respond when vital rates are perturbed. We used standardized vital rate estimates for 50 bird species to assess the use of phylogenetic imputation to fill gaps in demographic data. We calculated imputation accuracy for vital rates of focal species excluded from the data set either singly or in combination and with and without phylogeny, body mass, and life-history trait data. We used imputed vital rates to calculate demographic metrics, including generation time, to validate the use of imputation in demographic analyses. Covariance among vital rates and other trait data provided a strong basis to guide imputation of missing vital rates in birds, even in the absence of phylogenetic information. Mean NRMSE for null and phylogenetic models differed by <0.01 except when no vital rates were available or for vital rates with high phylogenetic signal (Pagel's λ > 0.8). In these cases, including body mass and life-history trait data compensated for lack of phylogenetic information: mean normalized root mean square error (NRMSE) for null and phylogenetic models differed by <0.01 for adult survival and <0.04 for maturation rate. Estimates of demographic metrics were sensitive to the accuracy of imputed vital rates. For example, mean error in generation time doubled in response to inaccurate estimates of maturation time. Accurate demographic data and metrics, such as generation time, are needed to inform conservation planning processes, for example through International Union for Conservation of Nature Red List assessments and population viability analysis. Imputed vital rates could be useful in this context but, as for any estimated model parameters, awareness of the sensitivities of demographic model outputs to the imputed vital rates is essential.

Cerrando Brechas en los Análisis Demográficos con Imputación Filogenética Resumen Los métodos de imputación guiados filogenéticamente se han aplicado con poca frecuencia para estimar los valores faltantes en los datos demográficos, aunque pueden ser una herramienta poderosa para la reconstrucción de tasas vitales de supervivencia, maduración y fecundidad de especies de importancia para la conservación. Las tasas vitales imputadas podrían usarse para generar parámetros en los modelos demográficos para explorar cómo responden las poblaciones cuando se perturban las tasas vitales. Utilizamos estimaciones de tasas vitales estandarizadas para 50 especies de aves para analizar el uso de la imputación filogenética para llenar los vacíos en los datos demográficos. Calculamos la certeza de imputación para las tasas vitales de las especies focales excluidas del conjunto de datos por sí solas o en combinación y con y sin datos de filogenia, masa corporal y características de historia de vida. Usamos las tasas vitales imputadas para calcular las medidas demográficas, incluyendo el tiempo de generación, y así validar el uso de la imputación en los análisis demográficos. La covarianza entre las tasas vitales y otros datos de características proporcionó una base sólida para orientar la imputación de tasas vitales faltantes en las aves, incluso la ausencia de información filogenética. El NRMSE medio para los modelos nulo y filogenético difirió por <0.01 salvo cuando no hubo tasas vitales disponibles o para tasas vitales con una señal filogenética alta (λ de Pagel > 0.8). En estos casos, la inclusión de la masa corporal y las características de historia de vida compensó la falta de información filogenética: el error cuadrático medio de la raíz normalizada media (NRMSE) para los modelos nulo y filogenéticos difirió por <0.01 para la supervivencia adulta y <0.04 para la tasa de maduración. Las estimaciones de las medidas demográficas fueron sensibles a la certeza de las tasas vitales imputadas. Por ejemplo, el error medio en el tiempo generacional se duplicó en respuesta a las estimaciones imprecisas del tiempo de maduración. Las medidas y datos demográficos certeros, como el tiempo generacional, son necesarios para orientar los procesos de planeación de la conservación; por ejemplo, a través de las valoraciones de la Lista Roja de la Unión Internacional para la Conservación de la Naturaleza y los análisis de viabilidad poblacional. Las tasas vitales imputadas podrían ser útiles en este contexto, pero como para cualquier tipo de parámetro de modelo estimado, el conocimiento de las sensibilidades del rendimiento del modelo demográfico es esencial para las tasas vitales imputadas.