Detecting turnover among complex communities using null models: a case study with sky-island haemosporidian parasites.

Turnover in species composition between sites, or beta diversity, is a critical component of species diversity that is typically influenced by geography, environment, and biotic interactions. Quantifying turnover is particularly challenging, however, in multi-host, multi-parasite assemblages where undersampling is unavoidable, resulting in inflated estimates of turnover and uncertainty about its spatial scale. We developed and implemented a framework using null models to test for community turnover in avian haemosporidian communities of three sky islands in the southwestern United States. We screened 776 birds for haemosporidian parasites from three genera (Parahaemoproteus, Plasmodium, and Leucocytozoon) by amplifying and sequencing a mitochondrial DNA barcode. We detected infections in 280 birds (36.1%), sequenced 357 infections, and found a total of 99 parasite haplotypes. When compared to communities simulated from a regional pool, we observed more unique, single-mountain haplotypes and fewer haplotypes shared among three mountain ranges than expected, indicating that haemosporidian communities differ to some degree among adjacent mountain ranges. These results were robust even after pruning datasets to include only identical sets of host species, and they were consistent for two of the three haemosporidian genera. The two more distant mountain ranges were more similar to each other than the one located centrally, suggesting that the differences we detected were due to stochastic colonization-extirpation dynamics. These results demonstrate that avian haemosporidian communities of temperate-zone forests differ on relatively fine spatial scales between adjacent sky islands. Null models are essential tools for testing the spatial scale of turnover in complex, undersampled, and poorly known systems.

Why are tropical mountain passes "low" for some species? Genetic and stable-isotope tests for differentiation, migration and expansion in elevational generalist songbirds.

Most tropical bird species have narrow elevational ranges, likely reflecting climatic specialization. This is consistent with Janzen's Rule, the tendency for mountain passes to be effectively "higher" in the tropics. Hence, those few tropical species that occur across broad elevational gradients (elevational generalists) represent a contradiction to Janzen's Rule. Here, we aim to address the following questions. Are elevational generalists being sundered by diversifying selection along the gradient? Does elevational movement cause these species to resist diversification or specialization? Have they recently expanded, suggesting that elevational generalism is short-lived in geological time? To answer these questions, we tested for differentiation, movement and expansion in four elevational generalist songbird species on the Andean west slope. We used morphology and mtDNA to test for genetic differentiation between high- and low-elevation populations. To test for elevational movements, we measured hydrogen isotope (δ2 H) values of metabolically inert feathers and metabolically active liver. Morphology differed for House Wren (Troglodytes aedon) and Hooded Siskin (Spinus magellanicus), but not for Cinereous Conebill (Conirostrum cinereum) and Rufous-collared Sparrow (Zonotrichia capensis) respectively. mtDNA was structured by elevation only in Z. capensis. δ2 H data indicated elevational movements by two tree- and shrub-foraging species with moderate-to-high vagility (C. cinereum and S. magellanicus), and sedentary behaviour by two terrestrial-foraging species with low-to-moderate vagility (T. aedon and Z. capensis). In S. magellanicus, elevational movements and lack of mtDNA structure contrast with striking morphological divergence, suggesting strong diversifying selection on body proportions across the c. 50 km gradient. All species except C. cinereum exhibited mtDNA haplotype variation consistent with recent population expansion across the elevational gradient, potentially concurrent with Holocene anthropogenic habitat conversion for agriculture. In different ways, each species defies the tendency for tropical birds to have long-term stable distributions and sedentary habits. We conclude that tropical elevational generalism is rare due to evolutionary instability.

Diversity, abundance, and host relationships of avian malaria and related haemosporidians in New Mexico pine forests.

Avian malaria and related haemosporidian parasites (genera Haemoproteus, Plasmodium, and Leucocytozoon) affect bird demography, species range limits, and community structure, yet they remain unsurveyed in most bird communities and populations. We conducted a community-level survey of these vector-transmitted parasites in New Mexico, USA, to describe their diversity, abundance, and host associations. We focused on the breeding-bird community in the transition zone between piñon-juniper woodland and ponderosa pine forests (elevational range: 2,150-2,460 m). We screened 186 birds representing 49 species using both standard PCR and microscopy techniques to detect infections of all three avian haemosporidian genera. We detected infections in 68 out of 186 birds (36.6%), the highest proportion of which were infected with Haemoproteus (20.9%), followed by Leucocytozoon (13.4%), then Plasmodium (8.0%). We sequenced mtDNA for 77 infections representing 43 haplotypes (25 Haemoproteus, 12 Leucocytozoon, 6 Plasmodium). When compared to all previously known haplotypes in the MalAvi and GenBank databases, 63% (27) of the haplotypes we recovered were novel. We found evidence for host specificity at the avian clade and species level, but this specificity was variable among parasite genera, in that Haemoproteus and Leucocytozoon were each restricted to three avian groups (out of six), while Plasmodium occurred in all groups except non-passerines. We found striking variation in infection rate among host species, with nearly universal infection among vireos and no infection among nuthatches. Using rarefaction and extrapolation, we estimated the total avian haemosporidian diversity to be 70 haplotypes (95% CI [43-98]); thus, we may have already sampled ∼60% of the diversity of avian haemosporidians in New Mexico pine forests. It is possible that future studies will find higher diversity in microhabitats or host species that are under-sampled or unsampled in the present study. Fortunately, this study is fully extendable via voucher specimens, frozen tissues, blood smears, parasite images, and documentation provided in open-access databases (MalAvi, GenBank, and ARCTOS).

Contribution of a mutational hot spot to hemoglobin adaptation in high-altitude Andean house wrens.

A key question in evolutionary genetics is why certain mutations or certain types of mutation make disproportionate contributions to adaptive phenotypic evolution. In principle, the preferential fixation of particular mutations could stem directly from variation in the underlying rate of mutation to function-altering alleles. However, the influence of mutation bias on the genetic architecture of phenotypic evolution is difficult to evaluate because data on rates of mutation to function-altering alleles are seldom available. Here, we report the discovery that a single point mutation at a highly mutable site in the ß(A)-globin gene has contributed to an evolutionary change in hemoglobin (Hb) function in high-altitude Andean house wrens (Troglodytes aedon). Results of experiments on native Hb variants and engineered, recombinant Hb mutants demonstrate that a nonsynonymous mutation at a CpG dinucleotide in the ß(A)-globin gene is responsible for an evolved difference in Hb-O2 affinity between high- and low-altitude house wren populations. Moreover, patterns of genomic differentiation between high- and low-altitude populations suggest that altitudinal differentiation in allele frequencies at the causal amino acid polymorphism reflects a history of spatially varying selection. The experimental results highlight the influence of mutation rate on the genetic basis of phenotypic evolution by demonstrating that a large-effect allele at a highly mutable CpG site has promoted physiological differentiation in blood O2 transport capacity between house wren populations that are native to different elevations.