Fine-scale genetic structure in the critically endangered red-fronted macaw in the absence of geographic and ecological barriers

Abstract

Behavioural and socio-cultural traits are recognized in the restriction of gene flow in species with high cognitive capacity and complex societies. This isolation by social barriers has been generally overlooked in threatened species by assuming disrupted gene flow due to population fragmentation and decline. We examine the genetic structure and ecology of the global population of the Critically Endangered red-fronted macaw (Ara rubrogenys), an endemic species to the inter-Andean valleys of Bolivia. We found a fine-scale genetic structuring in four genetic clusters. Genetic diversity was higher in wild compared to captive-bred macaws, but similar to that of captive wild-caught macaws. We found no clear evidence of severe genetic erosion in the population in recent decades, but it was patent in historic times, overlapping with drastic human habitat transformation and macaw persecution over millennia. We found no evidence of geographical and ecological barriers, owing to the high dispersal ability, nesting and foraging habits between genetic clusters. The lack of genetic intermixing despite long-distance foraging and seasonal movements suggests recruitment in natal colonies and other social factors reinforcing philopatry-related genetic structure. Conservation efforts should be specifically focussed on major threats in each genetic cluster as independent conservation units, and also considered in ex-situ management.

Figure 1

(a) Distribution range of the red-fronted macaw showing the sampled population nuclei (represented by letter codes: black letters for breeding nuclei, red letter for the single non-breeding area sampled) pooled in genetic clusters (represented by colours). The number of breeding pairs in each population nucleus at the time this study was conducted is represented by black numbers, while the maximum flock size in each breeding and non-breeding areas is represented by red numbers. Black points represent breeding colonies. (b) Distinct genetic clusters from the Bayesian clustering analysis with prior information on sampling location are shown for several K clusters. Each vertical line corresponds to one individual and the different colours represent the assignment to each cluster, with K = 4 as the optimal number of clusters estimated. Map was generated with ArcGIS 10.5 software (ESRI, Redland, USA, https://desktop.arcgis.com/en/) and modified with Microsoft PowerPoint 2010 (Microsoft Corporation, Redmond, WA, USA, https://www.microsoft.com/pt-pt/microsoft-365/previous-versions/office-2010), both software under CSIC Organizational License. Background was generated from Digital Elevation Model available from USGS (Global 30 Arc-Second Elevation, GTOPO30), freely available at https://www.usgs.gov/centers/eros/science/usgs-eros-archive-digital-elevation-global-30-arc-second-elevation-gtopo30?qt-science_center_objects=0#qt-science_center_objects. Author of the photograph: José L. Tella.

Figure 2

(a) Distinct genetic clusters from the Bayesian clustering analysis with prior information on sampling location are shown for several K clusters for captive red-fronted macaws, where the optimal number of clusters was estimated for K = 3. (b) Clustering analysis combining captive and wild individuals, where the optimal number of clusters was estimated for K = 5. Each vertical line corresponds to one individual and the different colours represent the assignment to each cluster. Colours assigned to each cluster correspond to the genetic clusters obtained for the wild population (see Fig. 1), except for the cluster C3 that cannot be assigned to any cluster in the wild.