Per J. Palsbøll

Reliability of genetic bottleneck tests for detecting recent population declines

The identification of population bottlenecks is critical in conservation because populations that have experienced significant reductions in abundance are subject to a variety of genetic and demographic processes that can hasten extinction. Genetic bottleneck tests constitute an appealing and popular approach for determining if a population decline has occurred because they only require sampling at a single point in time, yet reflect demographic history over multiple generations. However, a review of the published literature indicates that, as typically applied, microsatellite‐based bottleneck tests often do not detect bottlenecks in vertebrate populations known to have experienced declines. This observation was supported by simulations that revealed that bottleneck tests can have limited statistical power to detect bottlenecks largely as a result of limited sample sizes typically used in published studies. Moreover, commonly assumed values for mutation model parameters do not appear to encompass variation in microsatellite evolution observed in vertebrates and, on average, the proportion of multi‐step mutations is underestimated by a factor of approximately two. As a result, bottleneck tests can have a higher probability of ‘detecting’ bottlenecks in stable populations than expected based on the nominal significance level. We provide recommendations that could add rigor to inferences drawn from future bottleneck tests and highlight new directions for the characterization of demographic history.

Genetic tagging of humpback whales

The ability to recognize individual animals has substantially increased our knowledge of the biology and behaviour of many taxa. However, not all species lend themselves to this approach, either because of insufficient phenotypic variation or because tag attachment is not feasible. The use of genetic markers (‘tags’) represents a viable alternative to traditional methods of individual recognition, as they are permanent and exist in all individuals. We tested the use of genetic markers as the primary means of identifying individuals in a study of humpback whales in the North Atlantic Ocean. Analysis of six microsatellite loci, among 3,060 skin samples collected throughout this ocean allowed the unequivocal identification of individuals. Analysis of 692 ‘recaptures’, identified by their genotype, revealed individual local and migratory movements of up to 10,000 km, limited exchange among summer feeding grounds, and mixing in winter breeding areas, and also allowed the first estimates of animal abundance based solely on genotypic data. Our study demonstrates that genetic tagging is not only feasible, but generates data (for example, on sex) that can be valuable when interpreting the results of tagging experiments.

Population genetic structure of North Atlantic, Mediterranean Sea and Sea of Cortez fin whales, Balaenoptera physalus (Linnaeus 1758): analysis of mitochondrial and nuclear loci

Samples were collected from 407 fin whales, Balaenoptera physalus, at four North Atlantic and one Mediterranean Sea summer feeding area as well as the Sea of Cortez in the Pacific Ocean. For each sample, the sex, the sequence of the first 288 nucleotides of the mitochondrial (mt) control region and the genotype at six microsatellite loci were determined. A significant degree of divergence was detected at all nuclear and mt loci between North Atlantic/Mediterranean Sea and the Sea of Cortez. However, the divergence time estimated from the mt sequences was substantially lower than the time elapsed since the rise of the Panama Isthmus, suggesting occasional gene flow between the North Pacific and North Atlantic ocean after the separation of the two oceans. Within the North Atlantic and Mediterranean Sea, significant levels of heterogeneity were observed in the mtDNA between the Mediterranean Sea, the eastern (Spain) and the western (the Gulf of Maine and the Gulf of St Lawrence) North Atlantic. Samples collected off West Greenland and Iceland could not be unequivocally assigned to either of the two areas. The homogeneity tests performed using the nuclear data revealed significant levels of divergence only between the Mediterranean Sea and the Gulf of St Lawrence or West Greenland. In conclusion, our results suggest the existence of several recently diverged populations in the North Atlantic and Mediterranean Sea, possibly with some limited gene flow between adjacent populations, a population structure which is consistent with earlier population models proposed by Kellogg, Ingebrigtsen, and Sergeant.

DISCERNING BETWEEN RECURRENT GENE FLOW AND RECENT DIVERGENCE UNDER A FINITE-SITE MUTATION MODEL APPLIED TO NORTH ATLANTIC AND MEDITERRANEAN SEA FIN WHALE (BALAENOPTERA PHYSALUS) POPULATIONS

Abstract Genetic divergence among conspecific subpopulations can be due to either low recurrent gene flow or recent divergence and no gene flow. Here we present a modification of an earlier method developed by Nielsen and Wakeley (2001), which accommodates a finite‐site mutation model, to assess which of the two models of divergence is most likely given the observed data. We apply the method to nucleotide sequence data collected from the variable part of the mitochondrial control region in fin whales (Balaenoptera physalus) from the Atlantic coast off Spain and the Mediterranean Sea. Our estimations strongly favor a model of recurrent gene flow over a model of recent divergence and zero gene flow. We estimated the migration rate at two females per generation. While the estimated rate is high by evolutionary standards, exchange rates of this order of magnitude is low from an ecological and conservation perspective and entirely consistent with the current paucity of fin whale sightings in the Strait of Gibraltar today. Intensive commercial shore‐based whaling during the 1920s removed substantial numbers of fin whales in the Strait of Gibraltar and this local population has seemingly since failed to recover.

Radiation and speciation of pelagic organisms during periods of global warming: the case of the common minke whale, Balaenoptera acutorostrata

How do populations of highly mobile species inhabiting open environments become reproductively isolated and evolve into new species? We test the hypothesis that elevated ocean‐surface temperatures can facilitate allopatry among pelagic populations and thus promote speciation. Oceanographic modelling has shown that increasing surface temperatures cause localization and reduction of upwelling, leading to fragmentation of feeding areas critical to pelagic species. We test our hypothesis by genetic analyses of populations of two closely related baleen whales, the Antarctic minke whale (Balaenoptera bonaerensis) and common minke whale (Balaenoptera acutorostrata) whose current distributions and migration patterns extent are largely determined by areas of consistent upwelling with high primary production. Phylogeographic and population genetic analyses of mitochondrial DNA control‐region nucleotide sequences collected from 467 whales sampled in four different ocean basins were employed to infer the evolutionary relationship among populations of B. acutorostrata by rooting an intraspecific phylogeny with a population of B. bonaerensis. Our findings suggest that the two species diverged in the Southern Hemisphere less than 5 million years ago (Ma). This estimate places the speciation event during a period of extended global warming in the Pliocene. We propose that elevated ocean temperatures in the period facilitated allopatric speciation by disrupting the continuous belt of upwelling maintained by the Antarctic Circumpolar Current. Our analyses revealed that the current populations of B. acutorostrata likely diverged after the Pliocene some 1.5 Ma when global temperatures had decreased and presumably coinciding with the re‐establishment of the polar–equatorial temperature gradient that ultimately drives upwelling. In most population samples, we detected genetic signatures of exponential population expansions, consistent with the notion of increasing carrying capacity after the Pliocene. Our hypothesis that prolonged periods of global warming facilitate speciation in pelagic marine species that depend on upwelling should be tested by comparative analyses in other pelagic species.

CHARACTERIZING SOURCE–SINK DYNAMICS WITH GENETIC PARENTAGE ASSIGNMENTS

Source-sink dynamics have been suggested to characterize the population structure of many species, but the prevalence of source-sink systems in nature is uncertain because of inherent challenges in estimating migration rates among populations. Migration rates are often difficult to estimate directly with demographic methods, and indirect genetic methods are subject to a variety of assumptions that are difficult to meet or to apply to evolutionary timescales. Furthermore, such methods cannot be rigorously applied to high-gene-flow species. Here, we employ genetic parentage assignments in conjunction with demographic simulations to infer the level of immigration into a putative sink population. We use individual-based demographic models to estimate expected distributions of parent-offspring dyads under competing sink and closed-population models. By comparing the actual number of parent-offspring dyads (identified from multilocus genetic profiles) in a random sample of individuals taken from a population to expectations under these two contrasting demographic models, it is possible to estimate the rate of immigration and test hypotheses related to the role of immigration on population processes on an ecological timescale. The difference in the expected number of parent-offspring dyads between the two population models was greatest when immigration into the sink population was high, indicating that unlike traditional population genetic inference models, the highest degree of statistical power is achieved for the approach presented here when migration rates are high. We used the proposed genetic parentage approach to demonstrate that a threatened population of Marbled Murrelets (Braclhyrarmphus marmotus) appears to be supplemented by a low level of immigration (approximately 2-6% annually) from other populations.

Detecting populations in the 'ambiguous' zone: kinship-based estimation of population structure at low genetic divergence

Identifying population structure is one of the most common and important objectives of spatial analyses using population genetic data. Population structure is detected either by rejecting the null hypothesis of a homogenous distribution of genetic variation, or by estimating low migration rates. Issues arise with most current population genetic inference methods when the genetic divergence is low among putative populations. Low levels of genetic divergence may be as a result of either high ongoing migration or historic high migration but no current, ongoing migration. We direct attention to recent developments in the use of the tempo‐spatial distribution of closely related individuals to detect population structure or estimate current migration rates. These ‘kinship‐based’ approaches complement more traditional population‐based genetic inference methods by providing a means to detect population structure and estimate current migration rates when genetic divergence is low. However, for kinship‐based methods to become widely adopted, formal estimation procedures applicable to a range of species life histories are needed.

Genetic identification of a small and highly isolated population of fin whales (Balaenoptera physalus) in the Sea of Cortez, Mexico

For many years, researchers have speculatedthat fin whales are year-round residents in theSea of Cortez (= Gulf of California). Previouswork by Bérubé and co-workers has shownthat the degree of genetic diversity among finwhales in the Sea of Cortez at nuclear andmitochondrial loci is highly reduced. However,the relatively unobstructed connection with theNorth Pacific Ocean argues that Sea of Cortezfin whales are part of a much larger easternNorth Pacific population given the extensivemigratory ranges observed in fin whales andbaleen whales in general. The low degree ofgenetic variation might thus simply be due tohistoric fluctuations in the effectivepopulation size of an eastern North Pacificpopulation. In order to test if the reducedgenetic variation detected among fin whales inthe Sea of Cortez is due to small populationsize or a past bottleneck in an otherwise largeeastern North Pacific population, we analyzedthe geographic distribution of geneticvariation at a single mitochondrial (controlregion) and 16 nuclear loci in samplescollected from fin whales in the eastern NorthPacific (n = 12) as well as the Sea of Cortez(n = 77). Our results showed that fin whalesobserved in the Sea of Cortez constitute ahighly isolated and thus evolutionary uniquepopulation, which warrants special conservationmeasures given the current low estimate ofabundance of approximately 400 individuals.

Elevation and connectivity define genetic refugia for mountain sheep as climate warms

Global warming is predicted to affect the evolutionary potential of natural populations. We assessed genetic diversity of 25 populations of desert bighorn sheep (Ovis canadensis nelsoni) in southeastern California, where temperatures have increased and precipitation has decreased during the 20th century. Populations in low‐elevation habitats had lower genetic diversity, presumably reflecting more fluctuations in population sizes and founder effects. Higher‐elevation habitats acted as reservoirs of genetic diversity. However, genetic diversity was also affected by population connectivity, which has been disrupted by human development. Restoring population connectivity may be necessary to buffer the effects of climate change on this desert‐adapted ungulate.

Composition and possible function of social groupings of southern right whales in South African waters

We collected behavioural data and skin samples for molecular sex determination from 327 right whales (Eubalaena australis) in the coastal waters of South Africa between July and October, 1995 and 1996, as well as from 147 cows with calves-of-the-year between August and October 1996, September and November 1997. Data on group size, composition and behaviour were also available for 85 sightings of right whales south of 40degreesS. Although right whales are considered to be relatively non-social, only 23.3% of animals (apart from cow-calf pairs) encountered in South African waters were alone (N = 649), compared to 84.6% of animals seen south of 40degreesS in summer (N = 94). Of the pairs other than cows with calves encountered off South Africa, 31.0% (N = 58) were believed to be composed of cows with last-years calves (=yearlings): 93.3% (N = 15) of these yearlings were female, suggesting a possible mechanism for female philopatry. The incidence of these mother-yearling pairs dropped sharply after early August, indicating the abrupt weaning of some calves at an age of approximately one year. Most other animals were observed either in surface-active groups (SAGs) that indulged in apparent courtship behaviour, or in non-surface-active groups (non-SAGs). SAGs tended to be larger on average than non-SAGs (4.45 animals, N = 33, range 2-10, versus 2.57 animals, N = 108, range 2-5, respectively), and males predominated, while females predominated in non-SAGs. The number of animals participating per SAG increased through the season, whereas the size of non-SAGs remained constant. Given that most conceptions in southern right whales are estimated to occur in a 118-day period around mid-July, the observed increase in group size through late August and September may be due to declining availability of receptive females. Focal animals in SAGs proved to be predominantly female (83.3%, N = 24) and non-focal animals predominantly male (85.2%, N = 61): a few groups observed late in the winter season had a male rather than female focal animal. Sighting histories of the focal females revealed that none was seen with a calf in the 17 years that preceded the surveys, but four had been seen as calves, 2-5 (average 3.75) years previously. Six females were photographed with calves from 2 to 5 years after being the focal animal in a SAG, which is consistent with the observation that most focal females in SAGs were young, pre-pubertal animals, and therefore being the focal animal did not normally result in conception. It is still unclear where (and when) conceptions occur in southern right whales, but it is hypothesised that the focal females are practising a mating strategy in which the chances of conceiving with a larger male will be maximised. As neonatal survival is partly related to size, the female will in this way protect her substantial investment in time and energy represented by the calf.