Concerted evolution of duplicated mitochondrial control regions in three related seabird species

<p>Abstract</p> <p>Background</p> <p>Many population genetic and phylogenetic analyses of mitochondrial DNA (mtDNA) assume that mitochondrial genomes do not undergo recombination. Recently, concerted evolution of duplicated mitochondrial control regions has been documented in a range of taxa. Although the molecular mechanism that facilitates concerted evolution is unknown, all proposed mechanisms involve mtDNA recombination.</p> <p>Results</p> <p>Here, we document a duplication of a large region (cytochrome <it>b</it>, tRNA^Thr, tRNA^Pro, ND6, tRNA^Gluand the control region) in the mitochondrial genome of three related seabird species. To investigate the evolution of duplicate control regions, we sequenced both control region copies (CR1 and CR2) from 21 brown (<it>Sula leucogaster</it>), 21 red-footed (<it>S. sula</it>) and 21 blue-footed boobies (<it>S. nebouxii</it>). Phylogenetic analysis suggested that the duplicated control regions are predominantly evolving in concert; however, approximately 51 base pairs at the 5' end of CR1 and CR2 exhibited a discordant phylogenetic signal and appeared to be evolving independently.</p> <p>Conclusions</p> <p>Both the structure of the duplicated region and the conflicting phylogenetic signals are remarkably similar to a pattern found in <it>Thalassarche </it>albatrosses, which are united with boobies in a large clade that includes all procellariiform and most pelecaniform seabirds. Therefore we suggest that concerted evolution of duplicated control regions either is taxonomically widespread within seabirds, or that it has evolved many times.</p

Cryptic species and independent origins of allochronic populations within a seabird species complex (Hydrobates spp.)

Humans are inherently biased towards naming species based on morphological differences, which can lead to reproductively isolated species being mistakenly classified as one if they are morphologically similar. Recognising cryptic diversity is needed to understand drivers of speciation fully, and for accurate estimates of global biodiversity and assessments for conservation. We investigated cryptic species across the range of band-rumped storm-petrels (Hydrobates spp.): highly pelagic, nocturnal seabirds that breed on tropical and sub-tropical islands in the Atlantic and Pacific Oceans. In many breeding colonies, band-rumped storm-petrels have sympatric but temporally isolated (allochronic) populations; we sampled all breeding locations and allochronic populations. Using mitochondrial control region sequences from 754 birds, cytochrome b sequences from 69 birds, and reduced representation sequencing of the nuclear genomes of 133 birds, we uncovered high levels of genetic structuring. Population genomic analyses revealed up to seven unique clusters, and phylogenomic reconstruction showed that these represent seven monophyletic groups. We uncovered up to six independent breeding season switches across the phylogeny, spanning the continuum from genetically undifferentiated temporal populations to full allochronic species. Thus, band-rumped storm-petrels encompass multiple cryptic species, with non-geographic barriers potentially comprising strong barriers to gene flow

Reproductive Energetics and Prey Harvest of Leach's Storm-Petrels in the Northwest Atlantic

Leach's Storm—Petrels (Oceanodroma leucorhoa), the smallest and most abundant seabirds that breed in the northwest Atlantic, are not usually included in avian energetics models. To round out an energy analysis of seabirds spanning the full range of body sizes in the northwest Atlantic, the field metabolic rates (FMRs) of breeding Leach's Storm—Petrels were measured using doubly labeled water techniques (DLW). Metabolic, dietary and, demographic data were used as inputs in a populations energetics model to estimate the energy requirements and prey harvests of the Leach's Storm—Petrel population of eastern North America. FMRs of storm—petrels that remained in burrows averaged 83.3 ± 19.4 KJ/d. FMRs increased significantly with time (i.e., x in hours per day) at sea (y = [85.8 ± 6.5] + [3.13 ± 0.48]x), and metabolism at sea was estimated to be 161 ± 18 KJ/d. FMRs integrated over activity on land and activity at sea averaged 124 KJ/d during incubation and 142 KJ/d during chick rearing. Incubating adults weighed significantly more than adults rearing chicks, although adult mass did not vary with age of chick. Basal metabolic rate (BMR, measured as O2 flux) averaged 2.02 ± 1.01 cm3°g—1°h—1, equivalent to 45.4 ± 30.4 KJ/d, very similar to values obtained for breeding conspecifics in the Bay of Fundy and in the Bering Sea. Thermal conductance averaged 0.124 ± 0.065 cm3°g—1°h—1°°C—1. FMR/BMR ratios averaged 2.73 for incubating birds and 3.13 for birds rearing young. Population energetics modelling indicated that during a 7—mo breeding period Leach's Storm—Petrels at colonies in the northwest Atlantic Ocean consume >74 000 Mg of prey, mostly myctophids and amphipods (mostly Hyperia galba), as wall as euphausiids (mostly Meganyctiphanes norvegica) and other prey (decapods, copepods, isopods). Leach's Storm—Petrels make up °80% of the breeding seabird population in eastern Canada, but owing to small body size and metabolic efficiency, they account for comparatively little of the energy that flows through the avian assemblage of the northwest Atlantic. An intra—specific, inter—colony difference in FMR is suggested: FMRs measured in a Newfoundland colony were significantly higher than those determined with the same DLW procedure in the Bay of Fundy near the southern limit of the species' breeding range in the northwest Atlantic. Differences in ambient temperatures and wind speed associated with different oceanographic regimes may generate energetic differences. Like inter—colony differences in feeding ecology, inter—colony differences in FMR need to be considered in population and community energetics models and in meso— and mega—scale extrapolations

Activity-specific metabolic rates of free-living northern gannets and other seabirds

Field and activity-specific metabolic rates of 20 free-living Northern Gannets (Sula bassanus; mean mass = 3.21 kg) rearing chicks at Funk Island, Newfoundland, were measured using doubly labeled water and activity timers. Field metabolism (FMR) averaged 4865 kJ/d or 6.6 x basal metabolism (BMR). Regression analyses indicated a metabolic rate of 144 kJ/h while at the nest or on water, 349 kJ/h during flight, and 250 kJ/h during diurnal time at sea. These metabolic rates are high, probably because of costs of thermoregulation and flapping flight. BMR was slightly lower than predicted. Statistical analyses of metabolic rates of free-living seabirds indicated that rates are elevated in seabirds in cold-water regions and in seabirds that use flapping flight, but do not vary with phylogenetic order. FMR was correlated strongly with both BMR and metabolism at the nest. Population energy models may gain accuracy if metabolic rates are either expressed as multiples of metabolism at the nest or calculated from allometric equations appropriate for the species' activity pattern, oceanographic regime, and foraging mode

Population differentiation and evolution among thick-billed (Uria lomvia) and common murres (U. aalge)

The genetic structure of animal populations determines their potential for local adaptation and speciation. Most birds are highly mobile and accordingly have little genetic structuring, but some are strongly philopatric and exhibit substantial differentiation. In the present study, population differentiation and evolution were examined within two strongly philopatric seabird species, thick-billed (Uria lomvia) and common (U. ciat^e) murres, using morphometries, protein electrophoresis and nucleotide sequence analysis of amplified mitochondrial DNA (mtDNA). -- Four of five morphological measurements differed significantly both among three western Atlantic colonies of thick-billed murres, and between eastern and western Atlantic colonies. Electrophoretic analysis of 18 nuclear-encoded proteins indicated Utile genetic differentiation either among western Atlantic colonies, or across the Atlantic. Eighteen genotypes, defined by 16 variable nucleotide sites, were found within 253 base pairs (bp) of cytochrome b among 239 thick-billed murres from five Atlantic and two Pacific colonies. Significant genetic differentiation was found between Atlantic and Pacific thick-billed murres, concordant with geographic separation of the populations. Little genetic differentiation was found either among western Atlantic colonies, or across the Atlantic. The apparent genetic homogeneity of Atlantic colonies is inconsistent with evidence of strong natal philopatry and phenotypic differentiation of colonies, and may result from gene flow and/or recent colonizations by large founder populations. -- Common murres from Hornoya, Norway were significantly larger than those from Funk Island, Newfoundland in all of five dimensions. Ten genotypes, defined by 13 variable nucleotide sites, were found within 204 bp of cytochrome b among 142 common murres from four Atlantic and three Pacific colonies. Significant genetic differences were found between Atlantic and Pacific common murres, in accordance with their geographic separation. Genotype frequencies also varied clinally within the Atlantic. This cline is similar to a reported cline in the incidence of 'bridling' (a white sye ring and auricular grove) in common murres, and may have resulted from colonization of the Atlantic from two or more refugial centers following the Pleistocene glaciations. -- Little differentiation was found using morphometries or protein electrophoresis among thick-billed murres breeding at different sites within each of three colonies. However, cytochrome b genotype frequencies differed significantly both between two ledges in one area and among four areas at Hom0ya, Norway. Differentiation in mtDNA within Hornflya is consistent both with band returns, which indicate that murres often breed on their natal ledges, and with morphological evidence, which indicates that phenotypic differentiation exists within some colonies. -- Analyses of cytochrome b nucleotide sequences of six Atlantic alcid species, two gull species, two shorebird species and a dove revealed a preponderance of transitions over transversions, and of third position over first or second position substitutions. Saturation of transitions prevented phylogenetic analyses above the family level. Nonetheless, cladistic analysis of the alcid sequences supported previously suggested phytogenies in 1) grouping murre, razorbill (Alca torda) and dovekie (Alle alle) sequences, 2) clustering the black guillemot sequence with the murres, razorbill and dovekie, and 3) placing the Atlantic puffin (Fratercula arcticn) outside the other alcid sequences. The phylogenetic positions of the razorbill and dovekie relative to the murres could not be resolved. -- A review of mtDNA analyses indicated that genetic differentiation of populations and species is greater in freshwater and terrestrial species than in aerial or marine animals. This agrees with general dispersal capabilities, and probably relates to long-term effective population sizes. -- Key words: Alcidae; cytochrome b; morphometries; murrc; protein electrophoresis; polymerase chain reaction; review, Uria

Energy expenditures, activity budgets, and prey harvest of breding common murres

We used doubly labeled water and electronic timers to measure field metabolic rates (FMRs) and activity budgets of Common Murres (Uriu anlge) breeding in eastern Newfoundland. Mean FMR (1789 ± 265 kJ.day-I) was about 50% higher than predictions for seabirds. The high FMR may be related to thermal costs in a cold ocean environment and to high locomotion costs associated with a wing structure that is a compromise between flying and diving needs. Basal metabolic rates (X = 360 ± 69 kJ.day-1) were also higher than allometric predictions. While absent from the colony birds spent most (70.2-84.9%) time on the sea surface. Potential foraging range as estimated by flight time was greater during incubation than during chick rearing in two study years. Rates of prey exploitation were highest near the colony, but high exploitation rates may also have occurred about 60-70 km from the colony during incubation. Murres associated with the Witless Bay colony consumed an estimated 7579 tonnes of food, primarily capelin (M&lotus villosus)

Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms

Combination of the targeted amplification of nuclear introns and the analysis of single-stranded conformational polymorphisms has the potential to provide an inexpensive, rapid, versatile and sensitive genetic assay for evolutionary studies and conservation. We are developing primers and protocols to analyse nuclear introns in vertebrates, and are testing them in a population genetic study of marbled murrelets Brachyramphus marmoratus. Here we present protocols and results for introns for aldolase B, α-enolase, glyceraldehyde-3-phosphate dehydrogenase and lamin A. Results suggest that this approach presents a potentially powerful method for detecting genetic variation within and among local populations and species of animals: (i) a variety of genes can be surveyed, including genes of special interest such as those involved in disease resistance; (ii) assays are rapid and relatively inexpensive; (iii) large numbers of genes can be assayed, enabling accurate estimation of variation in the total genome; (iv) almost any mutation can be detected in the genes amplified; (v) the exact nature of variation can be investigated by sequence analysis if desired; (vi) statistical methods previously developed for proteins and/or sequence data can be used; (vii) protocols can be easily transferred to other species and other laboratories; and (viii) assays can be performed on old or degraded samples, blood or museum skins, so that animals need not be killed. Results of analyses for murrelets support earlier evidence that North American and Asiatic subspecies represent reproductively isolated species, and that genetic differences exist among murrelets from different sites within North America

Polymerase chain reaction (PCR) primers for the amplification of five nuclear introns in vertebrates

[Extract] Advancements in evolutionary genetics, as well as the conservation of biodiversity, increasingly require direct analyses of sequence variation in nuclear DNA. Recent studies indicate that nuclear introns have variabilities useful for both phylogenetics and population genetics (reviewed in Friesen 2000); however, use of introns is currently limited by the paucity of polymerase chain reaction (PCR) primers that have been demonstrated to have broad taxonomic utility (although several primers with less general or uncertain utilities have been published; reviewed in Friesen 2000). We have designed 30 general PCR primers for nuclear introns for vertebrates