Frank Hailer

Nuclear Genomic Sequences Reveal that Polar Bears Are an Old and Distinct Bear Lineage

Ancient Bears Polar bears are well known for adapting to their cold Arctic climate. Some recent studies, based on mitochondrial DNA, concluded that they are a relatively young species and that these adaptations occurred quite quickly. Although mitochondrial DNA is regularly used to estimate evolutionary history, it has some well-known drawbacks, including sex-biased dispersal and hybridization. Thus, Hailer et al. (p. 344) looked at neutral genetic data that are distributed more widely across the genome of a relatively large sample of polar, brown, and black bears. Consistent with fossil-based studies, the analysis reveals polar bears as a sister lineage to all brown bears, with an estimated divergence time of 300,000 to 900,000 years ago. Thus, polar bears are indeed of a more ancient lineage, and more recent estimates based on mitochondrial DNA are likely to have been affected by past hybridization with brown bear. Genomic analyses show that polar bears as a species are older and genetically more distinct than previously estimated. Recent studies have shown that the polar bear matriline (mitochondrial DNA) evolved from a brown bear lineage since the late Pleistocene, potentially indicating rapid speciation and adaption to arctic conditions. Here, we present a high-resolution data set from multiple independent loci across the nuclear genomes of a broad sample of polar, brown, and black bears. Bayesian coalescent analyses place polar bears outside the brown bear clade and date the divergence much earlier, in the middle Pleistocene, about 600 (338 to 934) thousand years ago. This provides more time for polar bear evolution and confirms previous suggestions that polar bears carry introgressed brown bear mitochondrial DNA due to past hybridization. Our results highlight that multilocus genomic analyses are crucial for an accurate understanding of evolutionary history.

Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline

Most of the white-tailed eagle (Haliaeetus albicilla) populations in Europe experienced dramatic declines during the twentieth century. However, owing to intense conservation actions and the ban of DDT and other persistent pollutants, populations are currently recovering. We show that despite passing through demographic bottlenecks, white-tailed eagle populations have retained significant levels of genetic diversity. Both genetic and ringing data indicate that migration between populations has not been a major factor for the maintenance of genetic variability. We argue that the long generation time of eagles has acted as an intrinsic buffer against loss of genetic diversity, leading to a shorter effective time of the experienced bottleneck. Notably, conservation actions taken in several small sub-populations have ensured the preservation of a larger proportion of the total genetic diversity than if conservation had focused on the population stronghold in Norway. For conservation programmes targeting other endangered, long-lived species, our results highlight the possibility for local retention of high genetic diversity in isolated remnant populations.

Intergenomic epistasis for fitness: within-population interactions between cytoplasmic and nuclear genes in Drosophila melanogaster.

The symbiotic relationship between the mitochondrial and nuclear genomes coordinates metabolic energy production and is fundamental to life among eukaryotes. Consequently, there is potential for strong selection to shape interactions between these two genomes. Substantial research attention has focused on the possibility that within-population sequence polymorphism in mitochondrial DNA (mtDNA) is maintained by mitonuclear fitness interactions. Early theory predicted that selection will often eliminate mitochondrial polymorphisms. However, recent models demonstrate that intergenomic interactions can promote the maintenance of polymorphism, especially if the nuclear genes involved are linked to the X chromosome. Most empirical studies to date that have assessed cytonuclear fitness interactions have studied variation across populations and it is still unclear how general and strong such interactions are within populations. We experimentally tested for cytonuclear interactions within a laboratory population of Drosophila melanogaster using 25 randomly sampled cytoplasmic genomes, expressed in three different haploid nuclear genetic backgrounds, while eliminating confounding effects of intracellular bacteria (e.g., Wolbachia). We found sizable cytonuclear fitness interactions within this population and present limited evidence suggesting that these effects were sex specific. Moreover, the relative fitness of cytonuclear genotypes was environment specific. Sequencing of mtDNA (2752 bp) revealed polymorphism within the population, suggesting that the observed cytoplasmic genetic effects may be mitochondrial in origin.

Hybridization among Three Native North American Canis Species in a Region of Natural Sympatry

Background Population densities of many species throughout the world are changing due to direct persecution as well as anthropogenic habitat modification. These changes may induce or increase the frequency of hybridization among taxa. If extensive, hybridization can threaten the genetic integrity or survival of endangered species. Three native species of the genus Canis, coyote (C. latrans), Mexican wolf (C. lupus baileyi) and red wolf (C. rufus), were historically sympatric in Texas, United States. Human impacts caused the latter two to go extinct in the wild, although they survived in captive breeding programs. Morphological data demonstrate historic reproductive isolation between all three taxa. While the red wolf population was impacted by introgressive hybridization with coyotes as it went extinct in the wild, the impact of hybridization on the Texas populations of the other species is not clear. Methodology/ Principal Findings We surveyed variation at maternally and paternally inherited genetic markers (mitochondrial control region sequence and Y chromosome microsatellites) in coyotes from Texas, Mexican wolves and red wolves from the captive breeding programs, and a reference population of coyotes from outside the historic red wolf range. Levels of variation and phylogenetic analyses suggest that hybridization has occasionally taken place between all three species, but that the impact on the coyote population is very small. Conclusion/Significance Our results demonstrate that the factors driving introgressive hybridization in sympatric Texan Canis are multiple and complex. Hybridization is not solely determined by body size or sex, and density-dependent effects do not fully explain the observed pattern either. No evidence of hybridization was identified in the Mexican wolf captive breeding program, but introgression appears to have had a greater impact on the captive red wolves.

Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle

The critically endangered Madagascar fish‐eagle (Haliaeetus vociferoides) is considered to be one of the rarest birds of prey globally and at significant risk of extinction. In the most recent census, only 222 adult individuals were recorded with an estimated total breeding population of no more than 100–120 pairs. Here, levels of Madagascar fish‐eagle population genetic diversity based on 47 microsatellite loci were compared with its sister species, the African fish‐eagle (Haliaeetus vocifer), and 16 of these loci were also characterized in the white‐tailed eagle (Haliaeetus albicilla) and the bald eagle (Haliaeetus leucocephalus). Overall, extremely low genetic diversity was observed in the Madagascar fish‐eagle compared to other surveyed Haliaeetus species. Determining whether this low diversity is the result of a recent bottleneck or a more historic event has important implications for their conservation. Using a Bayesian coalescent‐based method, we show that Madagascar fish‐eagles have maintained a small effective population size for hundreds to thousands of years and that its low level of neutral genetic diversity is not the result of a recent bottleneck. Therefore, efforts made to prevent Madagascar fish‐eagle extinction should place high priority on maintenance of habitat requirements and reducing direct and indirect human persecution. Given the current rate of deforestation in Madagascar, we further recommend that the population be expanded to occupy a larger geographical distribution. This will help the population persist when exposed to stochastic factors (e.g. climate and disease) that may threaten a species consisting of only 200 adult individuals while inhabiting a rapidly changing landscape.

Bears in a Forest of Gene Trees: Phylogenetic Inference Is Complicated by Incomplete Lineage Sorting and Gene Flow

Ursine bears are a mammalian subfamily that comprises six morphologically and ecologically distinct extant species. Previous phylogenetic analyses of concatenated nuclear genes could not resolve all relationships among bears, and appeared to conflict with the mitochondrial phylogeny. Evolutionary processes such as incomplete lineage sorting and introgression can cause gene tree discordance and complicate phylogenetic inferences, but are not accounted for in phylogenetic analyses of concatenated data. We generated a high-resolution data set of autosomal introns from several individuals per species and of Y-chromosomal markers. Incorporating intraspecific variability in coalescence-based phylogenetic and gene flow estimation approaches, we traced the genealogical history of individual alleles. Considerable heterogeneity among nuclear loci and discordance between nuclear and mitochondrial phylogenies were found. A species tree with divergence time estimates indicated that ursine bears diversified within less than 2 My. Consistent with a complex branching order within a clade of Asian bear species, we identified unidirectional gene flow from Asian black into sloth bears. Moreover, gene flow detected from brown into American black bears can explain the conflicting placement of the American black bear in mitochondrial and nuclear phylogenies. These results highlight that both incomplete lineage sorting and introgression are prominent evolutionary forces even on time scales up to several million years. Complex evolutionary patterns are not adequately captured by strictly bifurcating models, and can only be fully understood when analyzing multiple independently inherited loci in a coalescence framework. Phylogenetic incongruence among gene trees hence needs to be recognized as a biologically meaningful signal.

Hippoboscid-transmitted Haemoproteus parasites (Haemosporida) infect Galapagos Pelecaniform birds: Evidence from molecular and morphological studies, with a description of Haemoproteus iwa

Haemosporidian parasites are widely distributed and common parasites of birds, and the application of molecular techniques has revealed remarkable diversity among their lineages. Four haemosporidian genera infect avian hosts (Plasmodium, Haemoproteus, Leucocytozoon and Fallisia), and Haemoproteus is split into two sub-genera based on morphological evidence and phylogenetic support for two divergent sister clades. One clade (Haemoproteus (Parahaemoproteus)) contains parasites developing in birds belonging to several different orders, except pigeons and doves (Columbiformes), while the other (Haemoproteus (Haemoproteus)) has previously been shown to only infect dove hosts. Here we provide molecular and morphological identification of Haemoproteus parasites from several seabird species that are closely related to those found in dove hosts. We also document a deeply divergent clade with two haemosporidian lineages recovered primarily from frigatebirds (Fregatidae, Pelecaniformes) that is sister to the hippoboscid-(Hippoboscidae) transmitted dove parasites. One of the lineages in this new clade of parasites belongs to Haemoproteus iwa and is distributed in two species of frigatebird (Fregata) hosts from Hawaii, the Galapagos Islands, the eastern Pacific and throughout the Caribbean Basin. Haemosporidian parasites are often considered rare in seabirds due in part to the lack or low activity of some dipteran vectors (e.g., mosquitos, biting midges) in marine and coastal environments; however, we show that H. iwa is prevalent and is very likely vectored among frigatebirds by hippoboscid flies which are abundant on frigatebirds and other seabirds. This study supports the existence of two sister clades of avian Haemoproteus in accord with the subgeneric classification of avian hemoproteids. Description of H. iwa from Galapagos Fregata minor is given based on morphology of blood stages and segments of the mitochondrial cytochrome b gene, which can be used for identification. This study shows that hippoboscid flies warrant more attention as vectors of avian Haemoproteus spp., particularly in marine and coastal environments.

Assortative mating and fragmentation within dog breeds

BackgroundThere are around 400 internationally recognized dog breeds in the world today, with a remarkable diversity in size, shape, color and behavior. Breeds are considered to be uniform groups with similar physical characteristics, shaped by selection rooted in human preferences. This has led to a large genetic difference between breeds and a large extent of linkage disequilibrium within breeds. These characteristics are important for association mapping of candidate genes for diseases and therefore make dogs ideal models for gene mapping of human disorders. However, genetic uniformity within breeds may not always be the case. We studied patterns of genetic diversity within 164 poodles and compared it to 133 dogs from eight other breeds.ResultsOur analyses revealed strong population structure within poodles, with differences among some poodle groups as pronounced as those among other well-recognized breeds. Pedigree analysis going three generations back in time confirmed that subgroups within poodles result from assortative mating imposed by breed standards as well as breeder preferences. Matings have not taken place at random or within traditionally identified size classes in poodles. Instead, a novel set of five poodle groups was identified, defined by combinations of size and color, which is not officially recognized by the kennel clubs. Patterns of genetic diversity in other breeds suggest that assortative mating leading to fragmentation may be a common feature within many dog breeds.ConclusionThe genetic structure observed in poodles is the result of local mating patterns, implying that breed fragmentation may be different in different countries. Such pronounced structuring within dog breeds can increase the power of association mapping studies, but also represents a serious problem if ignored.In dog breeding, individuals are selected on the basis of morphology, behaviour, working or show purposes, as well as geographic population structure. The same processes which have historically created dog breeds are still ongoing, and create further subdivision within current dog breeds.

Long-term isolation of a highly mobile seabird on the Galapagos

The Galapagos Islands are renowned for their high degree of endemism. Marine taxa inhabiting the archipelago might be expected to be an exception, because of their utilization of pelagic habitats—the dispersal barrier for terrestrial taxa—as foraging grounds. Magnificent frigatebirds (Fregata magnificens) have a highly vagile lifestyle and wide geographical distribution around the South and Central American coasts. Given the potentially high levels of gene flow among populations, the species provides a good test of the effectiveness of the Galapagos ecosystem in isolating populations of highly dispersive marine species. We studied patterns of genetic (mitochondrial DNA, microsatellites and nuclear introns) and morphological variation across the distribution of magnificent frigatebirds. Concordant with predictions from life-history traits, we found signatures of extensive gene flow over most of the range, even across the Isthmus of Panama, which is a major barrier to gene flow in other tropical seabirds. In contrast, individuals from the Galapagos were strongly differentiated from all conspecifics, and have probably been isolated for several hundred thousand years. Our finding is a powerful testimony to the evolutionary uniqueness of the taxa inhabiting the Galapagos archipelago and its associated marine ecosystems.

Brown and Polar Bear Y Chromosomes Reveal Extensive Male-Biased Gene Flow within Brother Lineages

Brown and polar bears have become prominent examples in phylogeography, but previous phylogeographic studies relied largely on maternally inherited mitochondrial DNA (mtDNA) or were geographically restricted. The male-specific Y chromosome, a natural counterpart to mtDNA, has remained underexplored. Although this paternally inherited chromosome is indispensable for comprehensive analyses of phylogeographic patterns, technical difficulties and low variability have hampered its application in most mammals. We developed 13 novel Y-chromosomal sequence and microsatellite markers from the polar bear genome and screened these in a broad geographic sample of 130 brown and polar bears. We also analyzed a 390-kb-long Y-chromosomal scaffold using sequencing data from published male ursine genomes. Y chromosome evidence support the emerging understanding that brown and polar bears started to diverge no later than the Middle Pleistocene. Contrary to mtDNA patterns, we found 1) brown and polar bears to be reciprocally monophyletic sister (or rather brother) lineages, without signals of introgression, 2) male-biased gene flow across continents and on phylogeographic time scales, and 3) male dispersal that links the Alaskan ABC islands population to mainland brown bears. Due to female philopatry, mtDNA provides a highly structured estimate of population differentiation, while male-biased gene flow is a homogenizing force for nuclear genetic variation. Our findings highlight the importance of analyzing both maternally and paternally inherited loci for a comprehensive view of phylogeographic history, and that mtDNA-based phylogeographic studies of many mammals should be reevaluated. Recent advances in sequencing technology render the analysis of Y-chromosomal variation feasible, even in nonmodel organisms.