Population structure of nuclear and mitochondrial DNA variation among humpback whales in the North Pacific

Abstract

The population structure of variation in a nuclear actin intron and the control region of mitochondrial DNA is described for humpback whales from eight regions in the North Pacific Ocean: central California, Baja Peninsula, nearshore Mexico (Bahia Banderas), offshore Mexico (Socorro Island), southeastern Alaska, central Alaska (Prince Williams Sound), Hawaii and Japan (Ogasawara Islands). Primary mtDNA haplotypes and intron alleles were identified using selected restriction fragment length polymorphisms of target sequences amplified by the polymerase chain reaction (PCR-RFLP). There was little evidence of heterogeneity in the frequencies of mtDNA haplotypes or actin intron alleles due to the year or sex composition of the sample. However, frequencies of four mtDNA haplotypes showed marked regional differences in their distributions (phi ST = 0.277; P < 0.001; n = 205 individuals) while the two alleles showed significant, but less marked, regional differences (phi ST = 0.033; P < 0.013; n = 400 chromosomes). An hierarchical analysis of variance in frequencies of haplotypes and alleles supported the grouping of six regions into a central and eastern stock with further partitioning of variance among regions within stocks for haplotypes but not for alleles. Based on available genetic and demographic evidence, the southeastern Alaska and central California feeding grounds were selected for additional analyses of nuclear differentiation using allelic variation at four microsatellite loci. All four loci showed significant differences in allele frequencies (overall FST = 0.043; P < 0.001; average n = 139 chromosomes per locus), indicating at least partial reproductive isolation between the two regions as well as the segregation of mtDNA lineages. Although the two feeding grounds were not panmictic for nuclear or mitochondrial loci, estimates of long-term migration rates suggested that male-mediated gene flow was several-fold greater than female gene flow. These results include and extend the range and sample size of previously published work, providing additional evidence for the significance of genetic management units within oceanic populations of humpback whales.

Inferring sex-biased dispersal from population genetic tools: a review

“…For species in which females are philopatric and males disperse, genetic differentiation between populations is expected to be higher when estimated using mtDNA (or another maternal marker) than using a bi-parental marker. This prediction is consistent with many genetic analyses of dispersal patterns in species known to have male-biased dispersal (eg Melnick and Hoelzer, 1992;FitzSimmons et al, 1997;Rassmann et al, 1997;Baker et al, 1998).…”

“…This general approach has been applied to different vertebrate organisms including mammals (Melnick and Hoelzer, 1992;Baker et al, 1998;Seielstad et al, 1998;Pérez-Lezaun et al, 1999;Mesa et al, 2000;Escorza-Trevino and Dizon, 2000), birds (Guttierez, 1994;Gibbs et al, 2000;Piertney et al, 2000), reptiles (Karl et al, 1992;FitzSimmons et al, 1997;Rassmann et al, 1997) and fishes (Ferguson et al, 1993;Taylor et al, 1997;Patton et al, 1997). These different studies have employed several kinds of uni-parentally inherited markers (eg mtDNA, Ylinked markers).…”

Geographic variation of persistent organic pollutant levels in humpback whale (Megaptera novaeangliae) feeding areas of the North Pacific and North Atlantic

“…In general, humpback whales appear to be good bioindicators, reflecting what is known about environmental levels of contaminants. This lends further support to studies of humpback whale population structure, which have shown strong site fidelity of whales to feeding areas [10][11][12][13]. For example, whales that feed off the coasts of California, Oregon, and Washington are thought to form a relatively distinct feeding aggregation [10].…”

“…During their migration and winter breeding season in the tropics, humpback whales fast and depend on energy reserves accumulated in their blubber. Additionally, genetic and photoidentification studies give evidence of strong site fidelity of humpback whales to their feeding areas in both the North Pacific and North Atlantic [10][11][12][13]. Seasonal feeding behavior and fidelity to feeding regions provide the basis for using humpback whales to better understand regional patterns of marine pollution.…”

The effect of innovation and sex-specific migration on neutral cultural differentiation

“…As mitochondrial genes are inherited from the mother, even complete mixing of males among groups will not affect population structure if females are completely philopatric (Birky et al 1983;Chesser & Baker 1996;Prugnolle & de Meeus 2002). Empirical differences in maternally versus paternally inherited genetic markers have been used to infer the amount of sex-specific migration in humans (Seielstad et al 1998;Wilder et al 2004), chimpanzees (Langergraber et al 2007) and other animals (Baker et al 1998;Natoli et al 2005;Eriksson et al 2006), so similar questions could be addressed using F ST for cultural traits. While innovation may be analogous to mutation, it is unclear how closely the various well-studied models of mutation would correspond to innovation when a trait can have one of many variants or be completely absent.…”