Molecular insights into the historic demography of bowhead whales: understanding the evolutionary basis of contemporary management practices

Abstract

Patterns of genetic variation observed within species reflect evolutionary histories that include signatures of past demography. Understanding the demographic component of species' history is fundamental to informed management because changes in effective population size affect response to environmental change and evolvability, the strength of genetic drift, and maintenance of genetic variability. Species experiencing anthropogenic population reductions provide valuable case studies for understanding the genetic response to demographic change because historic changes in the census size are often well documented. A classic example is the bowhead whale, Balaena mysticetus, which experienced dramatic population depletion due to commercial whaling in the late 19th and early 20th centuries. Consequently, we analyzed a large multi-marker dataset of bowhead whales using a variety of analytical methods, including extended Bayesian skyline analysis and approximate Bayesian computation, to characterize genetic signatures of both ancient and contemporary demographic histories. No genetic signature of recent population depletion was recovered through any analysis incorporating realistic mutation assumptions, probably due to the combined influences of long generation time, short bottleneck duration, and the magnitude of population depletion. In contrast, a robust signal of population expansion was detected around 70,000 years ago, followed by a population decline around 15,000 years ago. The timing of these events coincides to a historic glacial period and the onset of warming at the end of the last glacial maximum, respectively. By implication, climate driven long-term variation in Arctic Ocean productivity, rather than recent anthropogenic disturbance, appears to have been the primary driver of historic bowhead whale demography.

Keywords: Approximate Bayesian computation; bottleneck; bowhead whale; generation time; historic demography; mutation rate..

Figure 1

Photograph of a bowhead whale taken near Point Barrow, Alaska in 2005 (photographer: J. C. George, Scientific Research Permit 782–1719). Note the whitish markings on the peduncle and scars on the back. Both are indications of advancing age. The maximum age of bowhead whales has been estimated at ∼200 year with an average age at sexual maturity >20 years.

Figure 2

Models of demographic history of bowhead whales tested through ABC.

Figure 3

Extended Bayesian skyline reconstructions of N_ef, timing of six past glacials (Rohling et al. ; gray bars denote glacials), CO2 (Petit et al. 1999), and CH4 (Loulergue et al. 2008) atmospheric concentrations plotted over time. For the demographic reconstruction, the gray area denotes the 95 highest posterior densities for the estimates, the hashed line represents the mean, and the solid line represents the median estimates.

Figure 4

Plots of the posterior estimates of N_e values and μ under various prior assumptions on N_e. There were five N_e priors with associated time priors defined for analysis (see Materials and Methods for details). The posterior estimates for these parameters are depicted in panels of the left column and N_{e(contempory)} = black line, N_{e(bottleneck)} = long dashes, N_e(historicA) = short dashes, and N_e(historicB) = dotted. The panels of the right column depict the posterior estimates for average μ, and the organization of panels within rows (a–d) corresponds to the prior bounds on N_e values that were assumed.

Figure 5

Box plots of heterozygosity values obtained through 1000 simulations for various combinations of N_{e(contemporary)}, N_e(historic), and generations since population reduction. The combination of parameters labeled 1-9 on the horizontal axis were 1 = 10,000, 50, 5; 2 = 10,000, 50, 50; 3 = 10,000, 50, 500; 4 = 10,000, 500, 5, 5 = 10,000, 500; 50; 6 = 10,000, 500, 500, 7 = 10,000, 1000, 5; 8 = 10,000, 1000, 50; and 9 = 10,000, 1000, 500, respectively. Error bars indicate maximum and minimum observed values, gray boxes are 50th and 75th percentiles, and the median value is denoted as a black horizontal line. Simulation 7 represented the combination of parameter values most similar to that postulated for the BCB stock of bowhead whales.