Assembly and RNA‐free annotation of highly heterozygous genomes: The case of the thick‐billed murre (Uria lomvia)

Thanks to a dramatic reduction in sequencing costs followed by a rapid development of bioinformatics tools, genome assembly and annotation have become accessible to many researchers in recent years. Among tetrapods, birds have genomes that display many features that facilitate their assembly and annotation, such as small genome size, low number of repeats and highly conserved genomic structure. However, we found that high genomic heterozygosity could have a great impact on the quality of the genome assembly of the thick‐billed murre (Uria lomvia), an arctic colonial seabird. In this study, we tested the performance of three genome assemblers, ray /sscape , soapdenovo 2 and platanus , in assembling the highly heterozygous genome of the thick‐billed murre. Our results show that platanus , an assembler specifically designed for heterozygous genomes, outperforms the other two approaches and produces a highly contiguous (N50 = 15.8 Mb) and complete genome assembly (93% presence of genes from the Benchmarking Universal Single Copy Ortholog [BUSCO] gene set). Additionally, we annotated the thick‐billed murre genome using a homology‐based approach that takes advantage of the genomic resources available for birds and other taxa. Our study will be useful for those researchers who are approaching assembly and annotation of highly heterozygous genomes, or genomes of species of conservation concern, and/or who have limited financial resources.     

Male-biased mutation rates and the overestimation of extrapair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia, Alcidae)

The widespread utility of hypervariable loci in genetic studies derives from the high mutation rate, and thus the high polymorphism, of these loci. Recent evidence suggests that mutation rates can be extremely high and may be male biased (occurring in the male germ-line). These two factors combined may result in erroneous overestimates of extrapair paternity, since legitimate offspring with novel alleles will have more mismatches with respect to the biological father than the biological mother. As mutations are male driven, increasing the number of hypervariable loci screened may simply increase the number of mismatches between fathers and their legitimate offspring. Here we describe a simple statistic, the probability of resemblance (PR), to distinguish between mismatches due to parental misassignment versus mutation in either sex or null alleles. We apply this method to parentage data on thick-billed murres (Uria lomvia), and demonstrate that, without considering either mutations or male-biased mutation rates, cases of extrapair paternity (7% in this study) would be grossly overestimated (14.5%-22%). The probability of resemblance can be utilized in parentage studies of any sexually reproducing species when allele or haplotype frequency data are available for putative parents and offspring. We suggest calculating this probability to correctly categorize legitimate offspring when mutations and null alleles may cause mismatches.     

Prey capture and selection throughout the breeding season in a deep‐diving generalist seabird,the thick‐billed murre

Generalist seabirds forage on a variety of prey items providing the opportunity to monitor diverse aquatic fauna simultaneously. For example, the coupling of prey consumption rates and movement patterns of generalist seabirds might be used to create three‐dimensional prey distribution maps (‘preyscapes’) for multiple prey species in the same region. However, the complex interaction between generalist seabird foraging behaviour and the various prey types clouds the interpretation of such preyscapes, and the mechanisms underlying prey selection need to be understood before such an application can be realized. Central place foraging theory provides a theoretical model for understanding such selectivity by predicting that larger prey items should be 1) selected farther from the colony and 2) for chick‐feeding compared with self‐feeding, but these predictions remain untested on most seabird species. Furthermore, rarely do we know how foraging features such as handling time, capture methods or choice of foraging location varies among prey types. We used three types of animal‐borne biologgers (camera loggers, GPS and depth‐loggers) to examine how a generalist Arctic seabird, the thick‐billed murre Uria lomvia, selects and captures their prey throughout the breeding season. Murres captured small prey at all phases of a dive, including while descending and ascending, but captured large fish mostly while ascending, with considerably longer handling times. Birds captured larger prey and dove deeper during chick‐rearing. As central place foraging theory predicted, birds travelling further also brought bigger prey items for their chick. The location of a dive (distance from colony and distance to shore) best explained which prey type was the most likely to get caught in a dive, and we created a preyscape surrounding our study colony. We discuss how these findings might aid the use of generalist seabirds as bioindicators.     

Genome‐scale sampling suggests cryptic epigenetic structuring and insular divergence in Canada lynx

Determining the molecular signatures of adaptive differentiation is a fundamental component of evolutionary biology. A key challenge is to identify such signatures in wild organisms, particularly between populations of highly mobile species that undergo substantial gene flow. The Canada lynx (Lynx canadensis) is one species where mainland populations appear largely undifferentiated at traditional genetic markers, despite inhabiting diverse environments and displaying phenotypic variation. Here, we used high‐throughput sequencing to investigate both neutral genetic structure and epigenetic differentiation across the distributional range of Canada lynx. Newfoundland lynx were identified as the most differentiated population at neutral genetic markers, with demographic modelling suggesting that divergence from the mainland occurred at the end of the last glaciation (20–33 KYA). In contrast, epigenetic structure revealed hidden levels of differentiation across the range coincident with environmental determinants including winter conditions, particularly in the peripheral Newfoundland and Alaskan populations. Several biological pathways related to morphology were differentially methylated between populations, suggesting that epigenetic modifications might explain morphological differences seen between geographically peripheral populations. Our results indicate that epigenetic modifications, specifically DNA methylation, are powerful markers to investigate population differentiation in wild and non‐model systems.     

Philopatry, kin clusters, and genetic relatedness in a population of woodrats (Neotoma macrotis)

Studies of highly kin-structured mammal societies have revealedthe importance of natal philopatry in determining the distributionof genetic variation within populations. In comparison, therelationship between philopatry and genetic diversity withinpopulations of moderately kin-structured societies has receivedrelatively little attention. Previous studies of Neotoma macrotishave suggested that females form distinct kin clusters. Eachkin cluster overlaps spatially with the home range(s) of oneor more males that are not related to each other or to the femaleswith which they are spatially associated. To examine interactionsbetween philopatry and genetic structure in this apparentlymoderately kin-structured species, we characterized spatialand genetic relationships among individually marked femalesin a population of N. macrotis from central coastal California.Our field studies revealed that, contrary to expectation, femalesin this population were not strongly philopatric and spatiallyclustered females were not characterized by high levels of geneticrelatedness. Nevertheless, genetic structure was evident withinthe study population; spatial and genetic distances among femaleswere significantly correlated, suggesting that dispersal patternsinfluenced genetic structure even in the absence of marked femalephilopatry. Because females with overlapping spatial distributionswere not typically closely related to one another, opportunitiesfor the evolution of kin-selected social behavior (e.g., cooperativecare of young) appear to be limited in this population.     

Population genetic structure in Atlantic and Pacific Ocean common murres (Uria aalge): natural replicate tests of post‐Pleistocene evolution

Understanding the factors that influence population differentiation in temperate taxa can be difficult because the signatures of both historic and contemporary demographics are often reflected in population genetic patterns. Fortunately, analyses based on coalescent theory can help untangle the relative influence of these historic and contemporary factors. Common murres (Uria aalge) are vagile seabirds that breed in the boreal and low arctic waters of the Northern Hemisphere. Previous analyses revealed that Atlantic and Pacific populations are genetically distinct; however, less is known about population genetic structure within ocean basins. We employed the mitochondrial control region, four microsatellite loci and four intron loci to investigate population genetic structure throughout the range of common murres. As in previous studies, we found that Atlantic and Pacific populations diverged during the Pleistocene and do not currently exchange migrants. Therefore, Atlantic and Pacific murre populations can be used as natural replicates to test mechanisms of population differentiation. While we found little population genetic structure within the Pacific, we detected significant east–west structuring among Atlantic colonies. The degree that population genetic structure reflected contemporary population demographics also differed between ocean basins. Specifically, while the low levels of population differentiation in the Pacific are at least partially due to high levels of contemporary gene flow, the east–west structuring of populations within the Atlantic appears to be the result of historic fragmentation of populations rather than restricted contemporary gene flow. The contrasting results in the Atlantic and Pacific Oceans highlight the necessity of carefully considering multilocus nonequilibrium population genetic approaches when reconstructing the demographic history of temperate Northern Hemisphere taxa.     

Trophic specialization in Arctic charr Salvelinus alpinus (Pisces; Salmonidae): morphological divergence and ontogenetic niche shifts

Lake Thingvallavatn supports four trophic morphs of Arctic charr, Salvelinus alpinus (L.); two of the morphs are benthic (small and large benthivorous charr) one exploits pelagic waters (planktivorous charr) and the fourth is found in both habitats (piscivorous charr). The morphological variation among these morphs was analysed by use of principal component analysis and canonical discriminant analysis. The benihic morphs have a short lower jaw and long pectoral fins. The benthic fish also have fewer gillrakers than the other morphs. Small and large benthivorous charrs attain sexual maturity from 2 and 6 years of age, and at fork lengths from 7 and 22 cm, respectively. Small benthivorous charr retain their juvenile parr marks as adults, have beige ventral colours, and are frequently melanized under the lower jaw. Planktivorous and piscivorous charr attain sexual maturity from 4 and 6 years of age, from fork lengths of 15 and 23 cm, respectively. This phenotypic polymorphism is associated with habitat utilization and diet of the fish, and has probably arisen within the lake system through diversification and niche specialization. The pelagic morphs apparently stem from a single population, and are possibly diversified through conditional niche shifts which affect ontogeny. Juveniles reaching a body length of 23 cm may change from zooplankton to fish feeding. Asymptotic length increases thereby from 20.5 cm in planktivorous charr to 30.2 cm in piscivorous charr. The benthic morphs appear to represent separate populations, although both feed chiefly on the gastropod Lymnaea peregra. Their co-existence seems to be facilitated by size dependent constraints on habitat use. The small morph (asymptotic length 13.3 cm) exploit the interstitial crevices in the lava block substratum, whereas the large morph (asymptotic length 55.4 cm) live epibenthically.     

Getting in shape: habitat‐based morphological divergence for two sympatric fishes

Freshwater fishes often show large amounts of body shape variation across divergent habitats and, in most cases, the observed differences have been attributed to the environmental pressures of living in lentic or lotic habitats. Previous studies have suggested a distinct set characters and morphological features for species occupying each habitat under the steady–unsteady swimming performance model. We tested this model and assessed body shape variation using geometric morphometrics for two widespread fishes, Goodea atripinnis (Goodeidae) and Chirostoma jordani (Atherinopsidae), inhabiting lentic and lotic habitats across the Mesa Central of Mexico. These species were previously shown to display little genetic variation across their respective ranges. Our body shape analyses reveal morphometric differentiation along the same axes for both species in each habitat. Both possess a deeper body shape in lentic habitats and a more streamlined body in lotic habitats, although the degree of divergence between habitats was less for C. jordani. Differences in the position of the mouth differed between habitats as well, with both species possessing a more superior mouth in lentic habitats. These recovered patterns are generally consistent with the steady–unsteady swimming model and highlight the significance of environmental forces in driving parallel body shape differences of organisms in divergent habitats. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 114 , 152–162.     

Identification of the maternal source of young‐of‐the‐year Arctic charr in Lake Hazen,Canada

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Population status of Common Guillemots Uria aalge at a colony in western Alaska: results and simulations

Colony-wide boat-based censuses suggest that numbers of Common Guillemots at Bluff, Alaska declined markedly in the late 1970s and remained low until 1983. Annual land-based counts of study plots since 1979 generally showed no trend. However, numbers declined substantially in one study area between 1978 and 1983. Reproductive success varied considerably among years and was highest in moderately warm summers. Simulation analyses suggest that the changes in numbers cannot be attributed to changes in reproductive success several years previously. Thus, factors affecting survival, presumably in winter, are apparently implicated in the declines.     

The Impact of male reproductive skew on kin structure and sociality in multi‐male groups

Patterns of within‐group relatedness are expected to affect the prospects for cooperation among group members through kin selection. It has long been established that dispersal patterns determine the availability of kin and there is ample evidence of matrilineal kin biases in social behavior across primate species. However, in 1979, Jeanne Altmann¹ suggested that mating patterns also influence the structure of within‐group relatedness; high male reproductive skew and the frequent replacement of breeding males leads to relatively high levels of paternal relatedness and age‐structured paternal sibships within groups. As a consequence of frequent replacement of breeding males, relatedness among offspring of a given female will be reduced to the half‐ rather than full‐sibling level. Depending on the number of sires and degree of relatedness among mothers, members of the same birth cohort may be as closely related as maternal siblings. If animals are able to recognize their paternal kin and exhibit biases in favor of them, this may influence the distribution of cooperation and the intensity of competition within groups of primates. Here, I summarize the evidence that serves as the basis for Altmann's predictions and review evidence regarding whether or not the availability of paternal kin also leads to paternal kin bias among primates.     

Inter‐seasonal persistence and size‐structuring of two minnow species within headwater streams in the Eastern Cape,South Africa

This study examined temporal variation in population dynamics and size structuring of two cyprinid minnows, Pseudobarbus afer and Barbus anoplus, in relation to their proximate physical habitats. Population estimates were determined using three‐pass depletion sampling during both summer and winter. The habitats were characterised by seasonal variation in all physico‐chemical conditions and spatial variation in substrata compositions. Whereas significant differences in population size were noted between seasons for B. anoplus, no differences were found between seasons for density and capture probability for either species. An increase in boulders was associated with increase in population size and density for P. afer; for B. anoplus, increased percentages of bedrock and bank vegetation were associated with an increase in population size and probability of capture, respectively. According to Canonical Correspondence Analysis, size structuring in P. afer was explained predominantly by seasonality, with smaller length classes associated with the seasonal variable of summer, while larger length classes were associated with pH that was higher in winter. By comparison, for B. anoplus, the habitat variables – bank vegetation and bedrock – accounted for much of the explained variance for size structuring. Recruitment appeared to be the major driver of size structuring for the two species; refugia, especially boulders and bank vegetation, also appeared to be important. Overall, the two species were adapted to the headwater streams that were generally variable in environmental conditions. Potential invasions by non‐native invasive fishes that occur within the mainstream habitats threaten these two species. Efforts should continue to protect these minnows from such invasions by constructing barriers to upstream migration of non‐native fishes into these headwater habitats.     

Indirect genetic effects in a sex‐limited trait: the case of breeding time in red‐billed gulls

Female reproductive performance can be strongly affected by male care, so that breeding time, a trait expressed only by females, can be seen as one trait determined by both male and female genotypes. Animal model analyses of a 46‐year study of red‐billed gulls (Larus novaehollandiae scopulinus) revealed that laying date was not heritable in females (h² = 0.001 ± 0.030), but significantly so in males (h² = 0.134 ± 0.029). Heritability of breeding time in males probably reflects genetic variability in some other trait such as courtship feeding ability. In line with predictions of evolutionary models incorporating indirect genetic effects, the strong and consistent directional selection for advanced breeding time has not resulted in detectable selection response in males. Our results demonstrate that a female trait is largely determined by genetic characteristics of its mate, and hence, any evolutionary change in red‐billed gull breeding time depends critically on genetic variation in males.     

The effects of heterospecifics and climatic conditions on incubation behavior within a mixed‐species colony

Parental incubation behavior largely influences nest survival, a critical demographic process in avian population dynamics, and behaviors vary across species with different life history breeding strategies. Although research has identified nest survival advantages of mixing colonies, behavioral mechanisms that might explain these effects is largely lacking. We examined parental incubation behavior using video‐monitoring techniques on Alcatraz Island, California, of black‐crowned night‐heron Nycticorax nycticorax (hereinafter, night‐heron) in a mixed‐species colony with California gulls Larus californicus and western gulls L. occidentalis. We first quantified general nesting behaviors (i.e. incubation constancy, and nest attendance), and a suite of specific nesting behaviors (i.e. inactivity, vigilance, preening, and nest maintenance) with respect to six different daily time periods. We employed linear mixed effects models to investigate environmental and temporal factors as sources of variation in incubation constancy and nest attendance using 211 nest days across three nesting seasons (2010–2012). We found incubation constancy (percent of time on the eggs) and nest attendance (percent of time at the nest) were lower for nests that were located < 3 m from one or more gull nest, which indirectly supports the predator protection hypothesis, whereby heterospecifics provide protection allowing more time for foraging and other self‐maintenance activities. To our knowledge, this is the first empirical evidence of the influence of one nesting species on the incubation behavior of another. We also identified distinct differences between incubation constancy and nest attentiveness, indicating that these biparental incubating species do not share similar energetic constraints as those that are observed for uniparental species. Additionally, we found that variation in incubation behavior was a function of temperature and precipitation, where the strength of these effects was dependent on the time of day. Overall, these findings strengthen our understanding of incubation behavior and nest ecology of a colonial‐nesting species.     

Division of labour and colony efficiency in social insects: effects of interactions between genetic architecture, colony kin structure and rate of perturbations

The efficiency of social insect colonies critically depends on their ability to efficiently allocate workers to the various tasks which need to be performed. While numerous models have investigated the mechanisms allowing an efficient colony response to external changes in the environment and internal perturbations, little attention has been devoted to the genetic architecture underlying task specialization. We used artificial evolution to compare the performances of three simple genetic architectures underlying within-colony variation in response thresholds of workers to five tasks. In the 'deterministic mapping' system, the thresholds of individuals for each of the five tasks is strictly genetically determined. In the second genetic architecture ('probabilistic mapping'), the genes only influence the probability of engaging in one of the tasks. Finally, in the 'dynamic mapping' system, the propensity of workers to engage in one of the five tasks depends not only on their own genotype, but also on the behavioural phenotypes of other colony members. We found that the deterministic mapping system performed well only when colonies consisted of unrelated individuals and were not subjected to perturbations in task allocation. The probabilistic mapping system performed well for colonies of related and unrelated individuals when there were no perturbations. Finally, the dynamic mapping system performed well under all conditions and was much more efficient than the two other mapping systems when there were perturbations. Overall, our simulations reveal that the type of mapping between genotype and individual behaviour greatly influences the dynamics of task specialization and colony productivity. Our simulations also reveal complex interactions between the mode of mapping, level of within-colony relatedness and risk of colony perturbations.     

Parallel and nonparallel ecological,morphological and genetic divergence in lake–stream stickleback from a single catchment

Parallel phenotypic evolution in similar environments has been well studied in evolutionary biology; however, comparatively little is known about the influence of determinism and historical contingency on the nature, extent and generality of this divergence. Taking advantage of a novel system containing multiple lake–stream stickleback populations, we examined the extent of ecological, morphological and genetic divergence between three‐spined stickleback present in parapatric environments. Consistent with other lake–stream studies, we found a shift towards a deeper body and shorter gill rakers in stream fish. Morphological shifts were concurrent with changes in diet, indicated by both stable isotope and stomach contents analysis. Performing a multivariate test for shared and unique components of evolutionary response to the distance gradient from the lake, we found a strong signature of parallel adaptation. Nonparallel divergence was also present, attributable mainly to differences between river locations. We additionally found evidence of genetic substructuring across five lake–stream transitions, indicating that some level of reproductive isolation occurs between populations in these habitats. Strong correlations between pairwise measures of morphological, ecological and genetic distance between lake and stream populations supports the hypothesis that divergent natural selection between habitats drives adaptive divergence and reproductive isolation. Lake–stream stickleback divergence in Lough Neagh provides evidence for the deterministic role of selection and supports the hypothesis that parallel selection in similar environments may initiate parallel speciation.     

Finding your mate in a seabird colony: contrasting strategies of the Guillemot Uria aalge and King Penguin Aptenodytes patagonicus

Capsule King Penguins recognize their mates by voice, but Guillemots do not need acoustic cues even though their calls show individual variation.

Aims To determine whether the structure of Guillemot calls could allow individual recognition, as with King Penguin, and whether acoustic cues are used to locate mates among a dense mass of conspecifics at a colony.

Methods Observations were made on breeding Guillemots and King Penguins. Calls made by birds returning to their mates were recorded, the signals digitized and the calls analysed. Calls were later played back to the mates of the birds concerned and the effects noted on both them and their neighbours.

Results Both Guillemots and King Penguins emitted calls on return to the breeding site which contained individual signatures and were therefore potentially usable for mate recognition. In King Penguins, auditory recognition was essential for finding a mate, whereas in Guillemots most of the arriving birds located their mate in a dense crowd of conspecifics without the help of acoustic signals. Guillemots could differentiate neighbours from strangers without auditory cues.

Conclusion Calls are essential for the successful identification of mates by King Penguins but not by Guillemots.     

Cryptic introgression between murre sister species (Uria spp.) in the Pacific low Arctic: frequency, cause, and implications

As southern species undergo northward range expansions, reports of hybridization between temperate and arctic taxa are increasing, which may have important implications for the evolution, conservation, and management of arctic species. The extent of hybridization between temperate common murres (Uria aalge) and arctic thick-billed murres (U. lomvia), seabirds in the family Alcidae, has been the subject of debate. In a previous survey of variation in mitochondrial DNA (mtDNA) in common and thick-billed murres sampled from throughout the North Pacific and low Arctic, 12 of 327 common murres (~4%) were found to possess DNA sequences characteristic of thick-billed murres. In the present study, we surveyed variation in three nuclear introns in 230 common murres and 56 thick-billed murres and report that these putative hybrids carry various combinations of intron alleles from common and thick-billed murres. Analysis using the program STRUCTURE indicated that nine of these individuals possessed high proportions of thick-billed murre intron alleles, two possessed alleles in F1 and F2 proportions, and one individual possessed predominantly common murre intron alleles. We propose that the asymmetric mtDNA introgression we observed is most likely the result of mate choice at mixed colonies based on differences in male mating behaviours. Our results highlight that hybridization between thick-billed and common murres is more prevalent than previously thought, which may have important implications for the conservation and management of arctic-dwelling thick-billed murres as common murres expand northward.