Timothy R. Frasier

related: an R package for analysing pairwise relatedness from codominant molecular markers.

Analyses of pairwise relatedness represent a key component to addressing many topics in biology. However, such analyses have been limited because most available programs provide a means to estimate relatedness based on only a single estimator, making comparison across estimators difficult. Second, all programs to date have been platform specific, working only on a specific operating system. This has the undesirable outcome of making choice of relatedness estimator limited by operating system preference, rather than being based on scientific rationale. Here, we present a new R package, called related, that can calculate relatedness based on seven estimators, can account for genotyping errors, missing data and inbreeding, and can estimate 95% confidence intervals. Moreover, simulation functions are provided that allow for easy comparison of the performance of different estimators and for analyses of how much resolution to expect from a given data set. Because this package works in R, it is platform independent. Combined, this functionality should allow for more appropriate analyses and interpretation of pairwise relatedness and will also allow for the integration of relatedness data into larger R workflows.

Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena )

Recent speciation events provide important insights into the understanding and conservation of Earths biodiversity, representing recent adaptations to a changing environment and an important source of future evolutionary potential. However, the most frequently applied criterion for molecular-based speciation investigations, that of reciprocal monophyly of mitochondrial sequences, overlooks recent speciation events where insufficient time has passed for fixed molecular differences to develop between putative species. Two morphologically distinguishable forms of finless porpoise (genus Neophocaena) exist in sympatry in the strait of Taiwan, however the taxonomic relationship of these different forms is controversial. To test the hypothesis that the two forms represent different species, a study was conducted based on morphological characters and microsatellite and mitochondrial markers. The data suggest that the two forms are highly differentiated in terms of both morphology and genetic characteristics, despite being sympatric, and therefore represent different species as defined by the biological species concept. Moreover, the two forms appear to have been reproductively isolated since sharing a common ancestor prior to the last major glaciation event ∼18 000 years ago. However, this represents an insufficient amount of time for reciprocal monophyly to have developed, and thus previous studies based on this criterion have overlooked this speciation event and resulted in incorrect taxonomic classification of these forms.

STORM: software for testing hypotheses of relatedness and mating patterns

Storm is a software package that allows users to test a variety of hypotheses regarding patterns of relatedness and patterns of mate choice and/or mate compatibility within a population. These functions are based on four main calculations that can be conducted either independently or in the hypothesis‐testing framework: internal relatedness; homozygosity by loci; pairwise relatedness; and a new metric called allele inheritance, which calculates the proportion of loci at which an offspring inherits a paternal allele different from that inherited from its mother. STORM allows users to test four hypotheses based on these calculations and Monte Carlo simulations: (i) are individuals within observed associations or groupings more/less related than expected; (ii) do observed offspring have more/less genetic variability (based on internal relatedness or homozygosity by loci) than expected from the gene pool; (iii) are observed mating pairs more/less related than expected if mating is random with respect to relatedness; and (iv) do observed offspring inherit paternal alleles different from those inherited from the mother more/less often than expected based on Mendelian inheritance.

Patterns of male reproductive success in a highly promiscuous whale species: the endangered North Atlantic right whale

Parentage analyses of baleen whales are rare, and although mating systems have been hypothesized for some species, little data on realized male reproductive success are available and the patterns of male reproductive success have remained elusive for most species. Here we combine over 20 years of photo‐identification data with high‐resolution genetic data for the majority of individual North Atlantic right whales to assess paternity in this endangered species. There was significant skew in male reproductive success compared to what would be expected if mating was random (P < 0.001). The difference was due to an excess of males assigned zero paternities, a deficiency of males assigned one paternity, and an excess of males assigned as fathers for multiple calves. The variance in male reproductive success was high relative to other aquatically mating marine mammals, but was low relative to mammals where the mating system is based on resource‐ and/or mate‐defence polygyny. These results are consistent with previous data suggesting that the right whale mating system represents one of the most intense examples of sperm competition in mammals, but that sperm competition on its own does not allow for the same degree of polygyny as systems where males can control access to resources and/or mates. The age distribution of assigned fathers was significantly biased towards older males (P < 0.05), with males not obtaining their first paternity until ~15 years of age, which is almost twice the average age of first fertilization in females (8 years), suggesting that mate competition is preventing younger males from reproducing. The uneven distribution of paternities results in a lower effective population size in this species that already has one of the lowest reported levels of genetic diversity, which may further inhibit reproductive success through mate incompatibility of genetically similar individuals.

Sources and Rates of Errors in Methods of Individual Identification for North Atlantic Right Whales

Abstract Many long-term studies of wildlife populations rely on individual identification based on natural markings or genetic profiling, or both. However, only rarely are these 2 independent data sets systematically compared with each other to estimate the error rates inherent in these studies. Here, >25 years of photo-identification data on the endangered North Atlantic right whale (Eubalaena glacialis) were compared with high-resolution genetic profiles, available for >75% of the individuals in the photo-identification catalog, in order to identify sources and rates of errors associated with both methods of individual identification. The resulting estimates were 0.0308 errors/identification for the photo-identification data, and 0.00121 errors/locus and 0.0327 errors/multilocus profile for the genetic data. These are among the lowest error rates yet reported, and indicate that the approaches used provide reliable means of individual identification for this species. However, despite these low error rates, the large size of the data sets results in a nonnegligible estimated number of errors, indicating that the potential for these errors needs to be incorporated into other analyses that are based on these data. A similar situation likely exists in other long-term studies where, although error rates are assumed to be low, the size of the data set results in a large number of errors that will influence subsequent analyses. Regularly conducting and reporting extensive database comparisons such as this is invaluable for maintaining the integrity of long-term data sets by identifying where sources of error are occurring and how protocols can be improved to lower error rates in the future.

Genetic connectivity among swarming sites in the wide ranging and recently declining little brown bat (Myotis lucifugus)

Characterizing movement dynamics and spatial aspects of gene flow within a species permits inference on population structuring. As patterns of structuring are products of historical and current demographics and gene flow, assessment of structure through time can yield an understanding of evolutionary dynamics acting on populations that are necessary to inform management. Recent dramatic population declines in hibernating bats in eastern North America from white-nose syndrome have prompted the need for information on movement dynamics for multiple bat species. We characterized population genetic structure of the little brown bat, Myotis lucifugus, at swarming sites in southeastern Canada using 9 nuclear microsatellites and a 292-bp region of the mitochondrial genome. Analyses of FST, ΦST, and Bayesian clustering (STRUCTURE) found weak levels of genetic structure among swarming sites for the nuclear and mitochondrial genome (Global FST = 0.001, P < 0.05, Global ΦST = 0.045, P < 0.01, STRUCTURE K = 1) suggesting high contemporary gene flow. Hierarchical AMOVA also suggests little structuring at a regional (provincial) level. Metrics of nuclear genetic structure were not found to differ between males and females suggesting weak asymmetries in gene flow between the sexes. However, a greater degree of mitochondrial structuring does support male-biased dispersal long term. Demographic analyses were consistent with past population growth and suggest a population expansion occurred from approximately 1250 to 12,500 BP, following Pleistocene deglaciation in the region. Our study suggests high gene flow and thus a high degree of connectivity among bats that visit swarming sites whereby mainland areas of the region may be best considered as one large gene pool for management and conservation.

Postcopulatory selection for dissimilar gametes maintains heterozygosity in the endangered North Atlantic right whale

Although small populations are expected to lose genetic diversity through genetic drift and inbreeding, a number of mechanisms exist that could minimize this genetic decline. Examples include mate choice for unrelated mates and fertilization patterns biased toward genetically dissimilar gametes. Both processes have been widely documented, but the long-term implications have received little attention. Here, we combined over 25 years of field data with high-resolution genetic data to assess the long-term impacts of biased fertilization patterns in the endangered North Atlantic right whale. Offspring have higher levels of microsatellite heterozygosity than expected from this gene pool (effect size = 0.326, P < 0.011). This pattern is not due to precopulatory mate choice for genetically dissimilar mates (P < 0.600), but instead results from postcopulatory selection for gametes that are genetically dissimilar (effect size = 0.37, P < 0.003). The long-term implication is that heterozygosity has slowly increased in calves born throughout the study period, as opposed to the slight decline that was expected. Therefore, this mechanism represents a natural means through which small populations can mitigate the loss of genetic diversity over time.

Cultural Hitchhiking in the Matrilineal Whales

Five species of whale with matrilineal social systems (daughters remain with mothers) have remarkably low levels of mitochondrial DNA diversity. Non-heritable matriline-level demography could reduce genetic diversity but the required conditions are not consistent with the natural histories of the matrilineal whales. The diversity of nuclear microsatellites is little reduced in the matrilineal whales arguing against bottlenecks. Selective sweeps of the mitochondrial genome are feasible causes but it is not clear why these only occurred in the matrilineal species. Cultural hitchhiking (cultural selection reducing diversity at neutral genetic loci transmitted in parallel to the culture) is supported in sperm whales which possess suitable matrilineal socio-cultural groups (coda clans). Killer whales are delineated into ecotypes which likely originated culturally. Culture, bottlenecks and selection, as well as their interactions, operating between- or within-ecotypes, may have reduced their mitochondrial diversity. The societies, cultures and genetics of false killer and two pilot whale species are insufficiently known to assess drivers of low mitochondrial diversity.

DNA profile of a sixteenth century western North Atlantic right whale (Eubalaena glacialis)

Low levels of genetic variability identified within the North Atlantic right whale (Eubalaena glacialis), when compared to the Southern right whale (E. australis) and other large whales, have been suggested to result from population reductions due to whaling. Previous genetic analysis of 218 whale bones from sixteenth century Basque whaling sites in the western North Atlantic revealed only a single right whale bone. We determined the genotypes of 27 microsatellite loci using DNA isolated from this bone. All alleles from the historic specimen occur in the extant western North Atlantic population and both the probability of identity of the specimen and the number of heterozygous loci are similar to that in the extant population. Assessments of how genetically different the historical population might have been suggest genetic characteristics have not changed substantially over four centuries of whaling.

Assessment of the extirpated Maritimes walrus using morphological and ancient DNA analysis

Species biogeography is a result of complex events and factors associated with climate change, ecological interactions, anthropogenic impacts, physical geography, and evolution. To understand the contemporary biogeography of a species, it is necessary to understand its history. Specimens from areas of localized extinction are important, as extirpation of species from these areas may represent the loss of unique adaptations and a distinctive evolutionary trajectory. The walrus (Odobenus rosmarus) has a discontinuous circumpolar distribution in the arctic and subarctic that once included the southeastern Canadian Maritimes region. However, exploitation of the Maritimes population during the 16th-18th centuries led to extirpation, and the species has not inhabited areas south of 55°N for ∼250 years. We examined genetic and morphological characteristics of specimens from the Maritimes, Atlantic (O. r. rosmarus) and Pacific (O. r. divergens) populations to test the hypothesis that the first group was distinctive. Analysis of Atlantic and Maritimes specimens indicated that most skull and mandibular measurements were significantly different between the Maritimes and Atlantic groups and discriminant analysis of principal components confirmed them as distinctive groups, with complete isolation of skull features. The Maritimes walrus appear to have been larger animals, with larger and more robust tusks, skulls and mandibles. The mtDNA control region haplotypes identified in Maritimes specimens were unique to the region and a greater average number of nucleotide differences were found between the regions (Atlantic and Maritimes) than within either group. Levels of diversity (h and π) were lower in the Maritimes, consistent with other studies of species at range margins. Our data suggest that the Maritimes walrus was a morphologically and genetically distinctive group that was on a different evolutionary path from other walrus found in the north Atlantic.