Integrated Environmental and Genomic Analysis Reveals the Drivers of Local Adaptation in African Indigenous Chickens.

Breeding for climate resilience is currently an important goal for sustainable livestock production. Local adaptations exhibited by indigenous livestock allow investigating the genetic control of this resilience. Ecological niche modeling (ENM) provides a powerful avenue to identify the main environmental drivers of selection. Here, we applied an integrative approach combining ENM with genome-wide selection signature analyses (XPEHH and Fst) and genotype-environment association (redundancy analysis), with the aim of identifying the genomic signatures of adaptation in African village chickens. By dissecting 34 agro-climatic variables from the ecosystems of 25 Ethiopian village chicken populations, ENM identified six key drivers of environmental challenges: One temperature variable-strongly correlated with elevation, three precipitation variables as proxies for water availability, and two soil/land cover variables as proxies of food availability for foraging chickens. Genome analyses based on whole-genome sequencing (n = 245), identified a few strongly supported genomic regions under selection for environmental challenges related to altitude, temperature, water scarcity, and food availability. These regions harbor several gene clusters including regulatory genes, suggesting a predominantly oligogenic control of environmental adaptation. Few candidate genes detected in relation to heat-stress, indicates likely epigenetic regulation of thermo-tolerance for a domestic species originating from a tropical Asian wild ancestor. These results provide possible explanations for the rapid past adaptation of chickens to diverse African agro-ecologies, while also representing new landmarks for sustainable breeding improvement for climate resilience. We show that the pre-identification of key environmental drivers, followed by genomic investigation, provides a powerful new approach for elucidating adaptation in domestic animals.

Optimizing design to estimate genetic correlations between environments with common environmental effects.

Breeding programs for different species aim to improve performance by testing members of full-sib (FS) and half-sib (HS) families in different environments. When genotypes respond differently to changes in the environment, this is defined as genotype by environment (G × E) interaction. The presence of common environmental effects within families generates covariance between siblings, and these effects should be taken into account when estimating a genetic correlation. Therefore, an optimal design should be established to accurately estimate the genetic correlation between environments in the presence of common environmental effects. We used stochastic simulation to find the optimal population structure using a combination of FS and HS groups with different levels of common environmental effects. Results show that in a population with a constant population size of 2,000 individuals per environment, ignoring common environmental effects when they are present in the population will lead to an upward bias in the estimated genetic correlation of on average 0.3 when the true genetic correlation is 0.5. When no common environmental effects are present in the population, the lowest standard error (SE) of the estimated genetic correlation was observed with a mating ratio of one dam per sire, and 10 offspring per sire per environment. When common environmental effects are present in the population and are included in the model, the lowest SE is obtained with mating ratios of at least 5 dams per sire and with a minimum number of 10 offspring per sire per environment. We recommend that studies that aim to estimate the magnitude of G × E in pigs, chicken, and fish should acknowledge the potential presence of common environmental effects and adjust the mating ratio accordingly.

The role of local adaptation in sustainable village chicken production.

Village chickens are ubiquitous in smallholder farming systems, contributing to household, local and national economies under diverse environmental, economic and cultural settings. However, they are raised in challenging environments where productivity is low while mortality is high. There is much interest in utilizing indigenous genetic resources to produce a chicken resilient to its environment, whilst providing the basis of an economically sustainable enterprise. Globally, however, a wide variety of interventions have so far proved unable to deliver sustainable improvements. Here, we show that regional differences in trait preferences and parasite burden are associated with distinct chicken genepools, likely in response to interacting natural and human-driven (economic and social) selection pressures. Drivers of regional differences include marketing opportunities, cultural preferences, agro-ecologies and parasite populations, and are evident in system adaptations, such as management practices, population dynamics and bird genotypes. Our results provide sound multidisciplinary evidence to support previous observations that sustainable poultry development interventions for smallholder farmers, including breeding programs, should be locally tailored and designed for flexible implementation.

Neutral and functionally important genes shed light on phylogeography and the history of high-altitude colonization in a widespread New World duck.

Phylogeographic studies often infer historical demographic processes underlying species distributions based on patterns of neutral genetic variation, but spatial variation in functionally important genes can provide additional insights about biogeographic history allowing for inferences about the potential role of adaptation in geographic range evolution. Integrating data from neutral markers and genes involved in oxygen (O2)-transport physiology, we test historical hypotheses about colonization and gene flow across low- and high-altitude regions in the Ruddy Duck (Oxyura jamaicensis), a widely distributed species in the New World. Using multilocus analyses that for the first time include populations from the Colombian Andes, we also examined the hypothesis that Ruddy Duck populations from northern South America are of hybrid origin. We found that neutral and functional genes appear to have moved into the Colombian Andes from both North America and southern South America, and that high-altitude Colombian populations do not exhibit evidence of adaptation to hypoxia in hemoglobin genes. Therefore, the biogeographic history of Ruddy Ducks is likely more complex than previously inferred. Our new data raise questions about the hypothesis that adaptation via natural selection to high-altitude conditions through amino acid replacements in the hemoglobin protein allowed Ruddy Ducks to disperse south along the high Andes into southern South America. The existence of shared genetic variation with populations from both North America and southern South America as well as private alleles suggests that the Colombian population of Ruddy Ducks may be of old hybrid origin. This study illustrates the breadth of inferences one can make by combining data from nuclear and functionally important loci in phylogeography, and underscores the importance of complete range-wide sampling to study species history in complex landscapes.

Genetic differentiation, niche divergence, and the origin and maintenance of the disjunct distribution in the Blossomcrown Anthocephala floriceps (Trochilidae).

Studies of the origin and maintenance of disjunct distributions are of special interest in biogeography. Disjunct distributions can arise following extinction of intermediate populations of a formerly continuous range and later maintained by climatic specialization. We tested hypotheses about how the currently disjunct distribution of the Blossomcrown (Anthocephala floriceps), a hummingbird species endemic to Colombia, arose and how is it maintained. By combining molecular data and models of potential historical distributions we evaluated: (1) the timing of separation between the two populations of the species, (2) whether the disjunct distribution could have arisen as a result of fragmentation of a formerly widespread range due to climatic changes, and (3) if the disjunct distribution might be currently maintained by specialization of each population to different climatic conditions. We found that the two populations are reciprocally monophyletic for mitochondrial and nuclear loci, and that their divergence occurred ca. 1.4 million years before present (95% credibility interval 0.7-2.1 mybp). Distribution models based on environmental data show that climate has likely not been suitable for a fully continuous range over the past 130,000 years, but the potential distribution 6,000 ybp was considerably larger than at present. Tests of climatic divergence suggest that significant niche divergence between populations is a likely explanation for the maintenance of their disjunct ranges. However, based on climate the current range of A. floriceps could potentially be much larger than it currently is, suggesting other ecological or historical factors have influenced it. Our results showing that the distribution of A. floriceps has been discontinous for a long period of time and that populations exhibit different climatic niches have taxonomic and conservation implications.