Habitat association constrains population history in two sympatric ovenbirds along Amazonian floodplains

Abstract

Aim Amazonian floodplains include distinct types of seasonally flooded habitats, determined by the flooding regime and sedimentation dynamics. Some bird species prefer specific habitat types within the floodplains. To investigate whether distinct habitats are differentially affected by geologic and climatic history, we compare population history in a sympatric and closely related pair of ovenbird species with different habitat associations. Location Amazonian floodplains. Taxa Synallaxis albigularis and Mazaria propinqua (Aves; Furnariidae). Methods Occurrence records were obtained from museums and public databases. Genomic data included nuclear loci (UCE) and the mitogenome for 49 samples. SNPs from UCE data were used to infer population genetic structure and effective migration. Mitogenomes were used to build phylogenetic trees and chronograms. Both datasets were used to infer historical demographic changes and test demographic scenarios. Results S. albigularis includes geographically structured mtDNA clades with a crown age of 250 ka, whereas M. propinqua includes a single clade with a crown age of 38 ka. Effective migration is lower at the base of the Andes for S. albigularis and at the lower Negro River for M. propinqua. Population expansion is detected for both species during the Quaternary, but was steeper and more recent in M. propinqua. Main conclusions The differences in population histories relate to distinct habitat associations along Amazonian floodplains. Preference of M. propinqua for more ephemeral island habitats may favour local extinctions, leading to demographic change, low genetic variability, no population structure and smaller effective population size. In contrast, more resilient habitats along the floodplains inhabited by S. albigularis may sustain local populations, generating and maintaining local diversity. Our results suggest that climatic variations of the late Pleistocene and Holocene caused changes in distribution and connectivity of the different types of habitats along the Amazonian floodplains, affecting gene flow and population sizes of associated bird populations.

Amazonian birds in more dynamic habitats have less population genetic structure and higher gene flow

“…Naka et al (2022) observed an individual of Mazaria propinqua , a species with a very low HWI value (10.8), swimming a few meters to reach a river island during a 100‐m dispersal experiment. More dramatically, an individual of this species was found on the Oyapok River in French Guiana (Ingels et al, 2012), 265 km from the nearest known population (Aguiar et al, 2010; Barbosa et al, 2022). Targeted searches along this river and in the intervening regions did not find populations of this species, supporting the hypothesis that this was a wandering individual (Ingels et al, 2012).…”

“…The extent of riverine island and floodplain forests has fluctuated over geological time with cycles of isolation and expansion on scales of tens to hundreds of thousands of years (Sawakuchi et al, 2022). Recent studies of historical demography in Amazonian floodplain birds indicate that species associated with riverine island habitats have gone through recent and steep demographic expansion in the Holocene when compared with floodplain forest specialists (Barbosa et al, 2022; Sawakuchi et al, 2022). This points to habitat‐level differences in historical demographics, driven by differences in sedimentation dynamics and habitat history (Sawakuchi et al, 2022).…”

“…In contrast, habitat preference was associated with the amount of population genetic structure (Bates et al, 2003;van Els et al, 2021). In Amazonian birds, Harvey et al (2017) found greater genetic structure in upland forest species than in floodplain forest species, and Barbosa et al (2022) found differences in structure between species in distinct habitats within Amazonian floodplains.…”

“…In contrast, habitat preference was associated with the amount of population genetic structure (Bates et al, 2003; van Els et al, 2021). In Amazonian birds, Harvey et al (2017) found greater genetic structure in upland forest species than in floodplain forest species, and Barbosa et al (2022) found differences in structure between species in distinct habitats within Amazonian floodplains. All these traits (canopy‐living, noninsectivorous diet, and floodplain habitat specialization) are correlated with reduced species richness in Amazonian birds (Salisbury et al, 2012), illustrating the potential long‐term evolutionary consequences of these aspects of life history.…”

“…Still, it is restricted to the river floodplain and is subdivided by the river itself. Multiple studies found that some Amazonian floodplain forest species had relatively high levels of genetic structure across their distribution but not between opposite banks of the same river (Barbosa et al, 2022; Luna et al, 2022; Silva et al, 2021). Corroborating the influence of habitat association of population history, Sawakuchi et al (2022) found distinct dates of demographic expansion for birds associated with riverine islands and floodplain forests in river margins, and that dates of demographic expansion for river island specialists agree with dates of sediment accumulation on riverine islands throughout Amazonia.…”