Speciation and population divergence in a mutualistic seed dispersing bird

Abstract

Bird-mediated seed dispersal is crucial for the regeneration and viability of ecosystems, often resulting in complex mutualistic species networks. Yet, how this mutualism drives the evolution of seed dispersing birds is still poorly understood. In the present study we combine whole genome re-sequencing analyses and morphometric data to assess the evolutionary processes that shaped the diversification of the Eurasian nutcracker (Nucifraga), a seed disperser known for its mutualism with pines (Pinus). Our results show that the divergence and phylogeographic patterns of nutcrackers resemble those of other non-mutualistic passerine birds and suggest that their early diversification was shaped by similar biogeographic and climatic processes. The limited variation in foraging traits indicates that local adaptation to pines likely played a minor role. Our study shows that close mutualistic relationships between bird and plant species might not necessarily act as a primary driver of evolution and diversification in resource-specialized birds.

Fig. 1. Genomic and morphometric analyses of the Eurasian nutcracker species complex.

a Species range according to Madge et al. and Gill et al. with sampling locations (black dots) of N. caryocatactes (northern) (N = 17), N. caryocatactes (southern) (N = 8) and N. multipunctata (N = 3). Subspecies distributions are depicted in different colours according to the legend. b Principal component analysis based on 110,979 SNPs separated the data in three distinct clusters. c Population structuring based on admixture analysis for K ranging from 2 to 4. Cross-validation indicates K = 3 as the optimal number of clusters. d Species tree under the Multiple Species Coalescence model constructed from 192 nuclear genomic alignments of 1 Mbp. e Linear discriminant analysis of phenotypic variation among Eurasian nutcrackers based on an independent morphometric dataset of 90 museum specimens. Bird images by Jon Baldur Hlidberg, courtesy of the authors.

Fig. 2. Evolutionary network of the four nutcracker species and their sisterspecies.

Phylogenetic network of the Eurasian nutcracker species complex based on 192 alignments of 1 Mbp of the nuclear genome. The numbers at the branches indicate the percentage of genomic alignments supporting the split. Some branch lengths are shortened for visualization purposes. Bird images by Jon Baldur Hlidberg, courtesy of the authors.

Fig. 3. Genetic and morphometric differentiation within the northern N. caryocatactes group.

a Distribution of the four subspecies within the northern N. caryocatactes group. Two specimens sampled in the range of N. c. caryocatactes were taxonomically and genetically identified as N. c. macrorhynchos. b PCA based on 142,799 SNPs separated the northern N. caryocatactes nutcrackers in three clusters. The specimen located in the middle of N. c. caryocatactes and N. c. macrorhynchos/N. c. japonica reflects a potential F1-hybrid. c Linear discriminant analyses based on morphometric measurements of 63 northern N. caryocatactes museum specimens. d Reconstruction of historical effective population size through time based on PSMC. N. c. rothschildi was excluded due to limited genome coverage.

Fig. 4. Genetic and morphometric differentiation within the southern N. caryocatactes group.

a Distribution of the four subspecies within the southern N. caryocatactes group. b Within-species genetic variation based on a PCA of 101,611 SNPs. c Linear discriminant analyses based on morphometric measurements of 23 southern N. caryocatactes museum specimens. N. c. interdicta had to be excluded due to lack of trait data. d Reconstruction of historical effective population size through time based on PSMC. N. c. hemispila was excluded from the analyses due to insufficient genome coverage.