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When the northern fulmar expanded its northeast Atlantic breeding range from the two known colonies, Grimsey in northern Iceland and St Kilda in the Outer Hebrides, Scotland, about 350 yr ago, the geographical pattern of colonisation – initially the Faroes, then Scotland, followed by Ireland and southern Britain – led James Fisher to propose a sole Icelandic source for the colonists. However, previously-analysed mitochondrial DNA from contemporary samples indicated a St Kildan origin for at least some colonists. If Fisher's hypothesis is correct and Iceland and not St Kilda was the source population for all of the new colonies, the Icelandic signal should be stronger in museum samples collected 100 yr ago when St Kilda was populated by people who harvested large numbers of fulmars. Patterns of genetic, specifically, nucleotide, diversity suggest an Icelandic origin for the pre-1940 samples. St Kilda birds contained a number of closely related haplotypes whereas Grimsey, Iceland, the other putative source population, contained diverse haplotypes. These two patterns are indicative of a younger and older population, respectively. When both nuclear aldolase and mitochondrial control region sequence data from historical samples collected on the newly colonized islands were examined, they contained highly divergent haplotypes characteristic of Grimsey, not St Kilda. Comparison of mitochondrial data from samples collected in the early and late 20th century showed an interesting pattern of haplotype turnover on St Kilda. Prior to 1940 the haplotypes present on St Kilda were genetically similar to one another, yet haplotype sampling in the 1990s showed highly divergent haplotypes on the island. We propose that these new haplotypes are not the result of mutation, but immigration from other colonies in the North Atlantic.
The northern fulmar Fulmarus glacialis, a medium-sized seabird with a distinctive tube-nose and opportunistic feeding habits (Hatch and Nettleship 1998), is a pelagic petrel that moults and over-winters in the open ocean and roams widely to forage during the breeding season. Today the species is ubiquitous across the North Atlantic, its range having expanded rapidly between the mid 18th century and the late 20th century (Fisher 1952a). Fisher (1952b) hypothesized the range expansion occurred in response to the increasing availability of scraps from the whaling industry and then of offal from expanding commercial fisheries. Alternatively, Salomonsen (1965) and Brown (1970) thought it was due to changes in oceanographic conditions.
The first record of an Atlantic breeding colony dates to the 1640s when nesting was recorded on Grimsey, an island north of Iceland (Fisher 1952a). The only other documented colony in the 17th century was on St Kilda in the Outer Hebrides, Scotland (Fisher and Waterston 1941). The large northern fulmar breeding population on St Kilda, which local residents harvested annually until 1930, remained stable throughout the initial range expansion and until about 1970 (Fisher 1952a, Lloyd et al. 1991). It then grew over the next 20 yr but has changed little since 1990 (Lloyd et al. 1991, Mitchell et al. 2004).
The historic spread of the northern fulmar to new colonies on Iceland and the eastern Atlantic has been described in meticulous detail (Fig. 1, Fisher 1952a). Following colonisation of the Faroe Islands between 1816 and 1839, the fulmar's range expanded to the British Isles and then to northwestern Europe. The path of expansion through the British Isles has been well documented, starting on Foula, Shetland Islands, followed by other sites in the Northern Isles, and then, more or less contemporaneously, sites bordering the Irish Sea to the west and the North Sea to the east. This geographical pattern led Fisher (1952a) to propose that, at least in the earlier stages, the expansion was driven by birds emigrating from Iceland colonizing islands as they moved in a southward direction.
Figure 1. Samples analyzed in this study and Burg et al. (2003) were obtained at the sites indicated by squares, while the two putative source populations of St Kilda and Grimsey are indicated by stars. Sites providing only contemporary samples (Burg et al. 2003) are indicated as white squares, sites providing both historical and contemporary samples are shown as grey squares, and sites providing only historical samples are shown as black squares. Sampling sites for the historic fulmars include St Kilda (StK), Fair Isle (FI), Orkney (Ork), Western Isles (WI), Coquet (Coq), Shetland Islands (Shet), Faroes (Far) and three sites in Iceland (Ice-N, Ice-S, Ice-G) including Grimsey. Contemporary only sampling sites in the North Atlantic include Ailsa (Ail), Ireland (Ire), southern Norway (Nor), Svalbard (Sval) and one site in Iceland (Ice-SW) and three sites in the Canadian Arctic: Prince Leopold (PL), Devin Island (DI) and Baffin Island (BI). Nor, Sval, PL, DI and BI sites from Kerr and Dove (2013) are not shown on the map. Dates beside Grimsey and St Kilda indicate the year since which occupation has been continuous. The number beside other sampling sites indicates the approximate date of colonisation (Fisher 1952b). Note that, although the Icelandic sampling site of Hvalfjordur (Ice-SW) was colonised in 1930, the Icelandic population expansion and colonisation of nearby sites started no later than 1753. Modified from Burg et al. (2003).
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To date, two studies have examined phylogeography of northern fulmars (Burg et al. 2003, Kerr and Dove 2013) and both showed little genetic differentiation among contemporary populations in the North Atlantic. Burg et al. (2003) used mitochondrial DNA (mtDNA) data from modern birds sampled from Iceland, Faroe Islands, Ireland and the British Isles in the late 1990s in an attempt to determine if birds from both Iceland and St Kilda or from Iceland alone contributed to the range expansion. The results from highly variable control region sequences indicated both St Kilda and Iceland contributed to the expansion, in contrast to Fisher's (1952a) scenario. However, pairwise comparisons within Burg et al.'s study did support one aspect of Fisher's hypothesis; the colonisation of the British Isles occurred in a “stepping stone” pattern, proceeding from one island to the next (Wright 1951).
The failure of modern samples to convincingly support Fisher's ‘out-of-Iceland’ hypothesis raised the possibility that any Icelandic signal might have been obscured by emigration of birds from St Kilda in the second half of the 20th century. If so, then samples obtained in the late 19th and early 20th century might reveal a different picture. At this time islanders still harvested about half the chicks, around 6000–10 000, reared on St Kilda each year (Lloyd et al. 1991). To test this idea we sampled fulmars in museum collections from Iceland, Faroes and Great Britain that had been collected between 1868 and 1939, approximately 30–100 yr before the period of population expansion on St Kilda (Lloyd et al. 1991). We hypothesised that these samples would show a genetic signature consistent with the out-of-Iceland hypothesis.
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We studied the patterns of genetic diversity in fulmar samples collected from breeding sites during the 1868–1939 breeding seasons in an attempt to determine if there was a genetic signature consistent with a single initial range expansion from Iceland. The pattern is not clear-cut and the data indicate three possibilities: 1) the observed high levels of mtDNA variation necessitate larger sample sizes to detect a convincing Icelandic signal; 2) St Kilda and Iceland both contributed to the initial expansion; or 3) Icelandic birds dispersed to St Kilda and other North Atlantic colonies prior to the main period of expansion. The three options are not mutually exclusive.
While the number of historical samples is limited, the fact that many of the haplotypes are found in several individuals, within the same time period and between periods, suggests that sample size is adequate to assess levels of variation present at the time. If it was not, then many more haplotypes would have been represented by single individuals. However, rare haplotypes are likely to be underrepresented due to the sample size. Sample size is more of a concern with the mtDNA data where higher levels of variation are present and this is supported by rarefaction curves where populations with less than seven samples and Grimsey (n = 10) have not levelled off (data not shown). For the less variable aldolase gene, the curves plateau much sooner, with the exception of Grimsey.
We now address the issue of gene flow between Iceland and St Kilda. Determining patterns of gene flow is difficult given the high diversity and complex haplotype network, particularly for the mtDNA data (Fig. 3). Historically St Kilda had unique mitochondrial haplotypes which are absent in contemporary samples and haplotypes that are now found at other sites (e.g. haplotype E), supporting the idea that gene flow was occurring between St Kilda and other colonies after the 1930s. The two main aldolase alleles (a and b) are also present on both St Kilda and Iceland; however, the fact that none of the remaining 24 alleles are present at multiple sites limits our conclusions. That alleles from historical samples are shared between Iceland and St Kilda for both markers suggest population connectivity between the two sites, but in what direction and when? Aldolase data show evidence of asymmetrical migration between Iceland and St Kilda. The levels of immigration to St Kilda are higher than emigration rates answering the question of directionality, but not the timing.
Historically haplotype diversity on St Kilda was comparable to levels found at some of the old colonies (e.g. Grimsey and Faroes); however, both mitochondrial and nuclear data show reduced nucleotide diversity on St Kilda relative to other colonies. Control region haplotypes on St Kilda are all separated by a single nucleotide substitution from haplotypes A and O (Fig. 2), which themselves are separated by a single mutation; and all but one of the seven aldolase alleles (Fig. 4) are a single step from allele a. This historical pattern is unique to St Kilda. In contrast, contemporary levels of genetic diversity on St Kilda are different: mtDNA haplotype diversity is much lower having decreased from 0.84 to 0.76 and nucleotide diversity increased (0.0056 to 0.0102). The divergent mtDNA haplotypes could not have been the result of mutation in such a short period of time and, as historical and contemporary sample sizes are similar (16 and 17 birds, respectively), sampling artefacts are unlikely to explain the difference in either diversity measure. One possible explanation is a selective sweep, yet this is not supported by the current data (Table 3). Alternatively if the population declined, haplotypes would have been lost (i.e. haplotype diversity reduced) through genetic drift and the loss would have been random. However, this still leaves the unanswered question of where did the divergent mtDNA haplotypes come from? As mentioned earlier, the historical and contemporary mtDNA haplotypes on St Kilda show some differences. Of the 12 mitochondrial haplotypes detected at any time on St Kilda, only two appear in both time series (haplotypes A and E). While some turnover in haplotypes occurred on the Faroe Islands, the only other site with comparable samples sizes in the two sampling periods, temporal differences in haplotypes on the Faroes are mainly due to the presence of eleven new haplotypes in the contemporary samples. In contrast, only two of the historical haplotypes sampled on St Kilda remain in the more contemporary samples. New, more divergent haplotypes (e.g. B and C) have appeared on St Kilda suggesting immigration to St Kilda. Immigration to St Kilda is supported by IMa results for the aldolase data.
The absence of long term isolation and presence of gene flow between St Kilda and other populations prior to the 1940s is evident in pairwise FST (Table 1) and the statistical parsimony network (Fig. 2). Prior to the 1940s, only two populations showed significant differences to St Kilda (Grimsey and Orkney) and each for a single locus.
Among the historical samples, a signal for population growth was detected in Iceland, Faroes, Orkney and St Kilda (Table 3, 4). Differences in marker variation and sample size may explain some of the differences between the aldolase and control region datasets. However, with the exception of northern Iceland, the two datasets show similar trends, with older colonies (Faroes, Iceland and St Kilda) exhibiting stronger and newer colonies weaker signals of population growth. These differences in the signal for historical population growth may reflect the amount of time since the colony was founded. A northern gannet Morus bassanus colony took almost 50 yr after founding for the colony to start growing (Siorat and Rocamora 1995). Fisher and Waterston's (1941) detailed study of the fulmar expansion shows some colonies took 15–30 yr before experiencing exponential growth while others remained small for much longer periods. Part of this lag time between founding and rapid increase in growth can be attributed to colony size and breeding success with larger colonies being more successful (Fisher and Waterston 1941, Fisher 1952b). Thus, while the long-established Icelandic colonies were growing, the more recently established colonies on the Northern Isles had perhaps not yet embarked on the phase of rapid growth. At the time the historical samples were collected, Faroe (1879–1928), Shetland (1905–1939) and Orkney (1906–1934) had been colonised for 40–112, 27–61 and 6–34 yr respectively.
Moving forward to the contemporary samples, the majority of the sites show population growth (Table 3), the exceptions being Ireland, a newer colony, and St Kilda. The fact that the genetic data do not show population growth at St Kilda at a time when independent colony counts indicate growth (1970–1990) suggests that the genetic tests are conservative. One interesting finding concerns changes in haplotypes. Haplotype diversity increased at both Faroe and Shetland. If migration rates fluctuated over time or birds were dispersing from islands with large colonies (e.g. Iceland) after 1940, this could explain these patterns.
The historical samples have shed light on the history of the fulmar expansion, but have not provided a conclusive answer to the out-of-Iceland hypothesis. In support, strong signals of population expansion and high haplotype/allelic and nucleotide diversity are evident in the historical samples from Iceland and indicative of an older population. In contrast, nucleotide diversity in historical samples from St Kilda is much lower, a pattern indicative of a relatively young, but isolated population. This is not to suggest St Kilda was colonized as recently as the other north Atlantic sites. Rather the colony may not be as old as the population on Grimsey, and the diverse haplotypes found on the newer colonies likely did not originate from St Kilda. Two other pieces of evidence support the out-of-Iceland hypothesis. First, the change in genetic diversity at St Kilda, where more divergent haplotypes are now present, suggests immigration to St Kilda. And second, haplotypes found at newer colonies are highly divergent and not characteristic of historical haplotypes present on St Kilda, but are typical of those from Iceland. However, we cannot rule out the possibility of emigration from St Kilda to the surrounding colonies.