Final Report Summary - BALTIC SEALS HISTORY (Tracking the impact of Holocene environmental change on the population genetics and demographics of four Baltic seal species)
Project objectives
The aim of this project was to understand the long-term dynamics of genetic and demographic changes in closely related species of seals inhabiting the same environment. We studied populations of four species that have inhabited the Baltic Sea; the extant ringed seal Phoca/Pusa hispida, grey seal Halichoerus grypus, and harbour seal Phoca vitulina, as well as the extinct harp seal Pagophilus groenlandicus. The aim of the project was achieved through: (I) reconstructing demographic and genetic changes in each population during the Holocene, using Bayesian coalescent inference from mtDNA sequences; (II) comparing the population dynamics of the four species in the context of climate change, human exploitation, and their respective life histories; (III) reconstructing the evolutionary and demographic processes leading to the extinction of the Baltic harp seal, in comparison with the demographic changes in populations of the three extant Baltic seal species.
Results
We analysed genetic variability in mtDNA (mitochondrial DNA) control region in 76 ancient samples of Baltic seals, 187 historical samples (from the period 1827-1990), and 97 contemporary samples (from the period 1993-2012). The ancient samples belonged to all four Baltic species, while historical and contemporary samples belonged to the tree extant species. The historical samples included 12 harp seals from the coast of the Barents Sea, used for the comparison with the Baltic harp seals. We also obtained mtDNA control region sequences from 202 individuals of Baltic seals from Genbank, which were included into the data analysis. For the ancient and modern harp seals, we additionally amplified a 298 base pair sequence of cytochrome b gene, and obtained 40 additional sequences from Genbank. The subfossil samples that were successfully sequenced dated between 2900 and 13 710 uncalibrated radiocarbon years B.P. Additionally, among the ancient samples there were four samples from two medieval archaeological sites (AD 1050-1255) from Gdansk, Poland.
Our results confirmed the presence of the harp seal in different parts of the Baltic Sea during the Holocene. The harp seal population had a recent origin in the Baltic Sea, which allowed us to reconstruct its dynamics from the time of its founding to its extinction. The Baltic harp seal population was established no earlier than after the formation of the Baltic Sea about 8000 years ago, and was believed to become extinct from the Baltic Sea at the end of the Subboreal period about 2500 years ago (Storå and Ericson 2004). However, our genetic analysis identified the four medieval samples from Poland as the harp seals, moving the harp seal extinction date at least 1500 years later. The reconstruction of the harp seal population dynamics in the Baltic Sea and Skagerrak/Kattegat straits using the Bayesian Skyline Plot method suggests fast population growth about 6500 years ago, consistent with the time of the establishment of the Baltic population inferred from the distribution of radiocarbon dated seal bones. The analysis of phylogenetic relationships between the extinct Baltic harp seals and extant harp seals from the North Atlantic showed that the Baltic population was established by a large and diverse founder population. The pattern of haplotype sharing suggests that the founder population most likely originated from the White Sea breeding colony, which is spatially closest. The reconstruction of the harp seal population dynamics also suggests that this population declined abruptly about 1000 years ago, which coincided with the Medieval Warm Period (AD 950-1250).
Nucleotide diversity of the ancient harp seals in mtDNA control region was comparable with the ancient ringed seals (the most numerous seal species in the Baltic at present) and higher than grey seals and harbour seals. This suggests that the harp seal population declined from numbers comparable with the most numerous seal species in the Baltic Sea to extinction within a period of several hundred years. Possible causes of such decline include climate-related environmental change, overhunting, competition with other seal species, and inbreeding due to genetic isolation. Our results allow us to exclude the last potential cause, as genetic diversity of harp seal in the small Baltic Sea basin was higher than in two Northwest Atlantic breeding colonies, while the population numbers in the entire Northwest Atlantic were estimated at 4.5 million. Climate-related environmental change could have caused the extinction of this ice-breeding species, as the Baltic Sea was the southernmost part of its range. However, throughout its history this population survived warmer temperatures than in the time of its extinction, so climate warming is unlikely to be the main cause of the extinction. However, the decline of the harp seal population also coincided with the decline in the salinity of the Baltic Sea, which implies the decline in sea productivity. This could have intensified competition for food resources with other seal species, as well as with humans. Competition with another seal species would have resulted in population growth of these species after the harp seal extinction. Indeed, the grey seal shows a strong signal of population growth about 500 years ago, while the last known record of the harp seal dates for about 700 years ago. Therefore, it is likely that competition with the grey seal contributed to the harp seal extinction. The effect of hunting by humans is more difficult to assess. However, widespread presence of harp seals in archaeological record (Storå and Ericson 2004) combined with the significant increase in human population size in the Baltic Sea region during the Medieval Warm Period (Tallavaara and Seppa 2012) suggest that hunting could have contributed to the harp seal extinction.
Our research also provides the first data on the genetic variability of ancient (13710- 2900 years before present) and historical, pre-bottleneck populations (from the period 1843-1990) of each of the three extant seal species, and reconstruction of effective population sizes. The ringed seal had consistently highest and the harbour seal lowest effective size. Our results also suggest extensive gene flow among different regions of the Baltic Sea, as well as between the Baltic and Skagerrak/Kattegat straits. The reconstruction of Holocene population dynamics for the ringed seal and harbour seal suggests population growth throughout the entire period studied, until modern times. The same reconstruction for the grey seal suggests low effective population size until about 500 years ago, when a sudden population growth was observed, followed by a decline in the XX century. The comparison of modern pre-bottleneck and post-bottleneck populations showed a decline in haplotype diversity in each extant species.
Conclusions
The reconstruction of the demographic changes in the Baltic harp seal population suggests that it had high effective size throughout most of its history, and declined abruptly towards extinction. Although this decline coincided with the Medieval Warm Period, climate warming is unlikely to be the major cause of the extinction, as no effects of earlier periods of climate warming were reflected in the population dynamics. We also did not find any clear effects of climatic fluctuations on population dynamics of other seal species. The Baltic seals, including two exclusively ice-breeding species (the harp seal and the ringed seal) seem to be surprisingly resilient to climate-induced environmental change. In contrast, the recent severe population decline in all three extant species showed that they are vulnerable to hunting, and it is likely that overhunting contributed to the harp seal extinction. Moreover, the comparison of population dynamics patterns in the four Baltic seal species suggest that the harp seal extinction could have been partially caused by competition with the grey seal, which was likely intensified by a decline in sea salinity and a resulting decline in sea productivity.
Potential applications and impact
The results of this project contribute to a better understanding of the processes underlying population extinction or survival, which is a fundamental question of evolutionary biology with very important practical implications for biodiversity conservation. Besides contributing to the general knowledge in the area of evolutionary and conservation biology, this project can be also applied to a particular case of conservation of seals in the Baltic Sea. Our results suggest that climate change was not a major driver of population dynamics of Baltic seals, including the two exclusively ice-breeding species, which has important conservation implications. The knowledge obtained in this project may be applied towards the development of predictive models on the impact of on-going human activities (including culling) and climate change on the Baltic seals, which will help to develop effective strategies for their conservation. This will contribute to the implementation of the European Union's Marine Strategy and the Baltic Sea Action Plan of the Helsinki Commission.
References
Storå J, Ericson PGP (2004) A prehistoric breeding population of harp seals (Phoca groenlandica) in the Baltic Sea. Mar. Mamm. Sci. 20: 115-133.
Tallavaara M, Seppa H (2012) Did the mid-Holocene environmental changes cause the boom and bust of hunter-gatherer population size in eastern Fennoscandia? The Holocene 22: 215225.
The aim of this project was to understand the long-term dynamics of genetic and demographic changes in closely related species of seals inhabiting the same environment. We studied populations of four species that have inhabited the Baltic Sea; the extant ringed seal Phoca/Pusa hispida, grey seal Halichoerus grypus, and harbour seal Phoca vitulina, as well as the extinct harp seal Pagophilus groenlandicus. The aim of the project was achieved through: (I) reconstructing demographic and genetic changes in each population during the Holocene, using Bayesian coalescent inference from mtDNA sequences; (II) comparing the population dynamics of the four species in the context of climate change, human exploitation, and their respective life histories; (III) reconstructing the evolutionary and demographic processes leading to the extinction of the Baltic harp seal, in comparison with the demographic changes in populations of the three extant Baltic seal species.
Results
We analysed genetic variability in mtDNA (mitochondrial DNA) control region in 76 ancient samples of Baltic seals, 187 historical samples (from the period 1827-1990), and 97 contemporary samples (from the period 1993-2012). The ancient samples belonged to all four Baltic species, while historical and contemporary samples belonged to the tree extant species. The historical samples included 12 harp seals from the coast of the Barents Sea, used for the comparison with the Baltic harp seals. We also obtained mtDNA control region sequences from 202 individuals of Baltic seals from Genbank, which were included into the data analysis. For the ancient and modern harp seals, we additionally amplified a 298 base pair sequence of cytochrome b gene, and obtained 40 additional sequences from Genbank. The subfossil samples that were successfully sequenced dated between 2900 and 13 710 uncalibrated radiocarbon years B.P. Additionally, among the ancient samples there were four samples from two medieval archaeological sites (AD 1050-1255) from Gdansk, Poland.
Our results confirmed the presence of the harp seal in different parts of the Baltic Sea during the Holocene. The harp seal population had a recent origin in the Baltic Sea, which allowed us to reconstruct its dynamics from the time of its founding to its extinction. The Baltic harp seal population was established no earlier than after the formation of the Baltic Sea about 8000 years ago, and was believed to become extinct from the Baltic Sea at the end of the Subboreal period about 2500 years ago (Storå and Ericson 2004). However, our genetic analysis identified the four medieval samples from Poland as the harp seals, moving the harp seal extinction date at least 1500 years later. The reconstruction of the harp seal population dynamics in the Baltic Sea and Skagerrak/Kattegat straits using the Bayesian Skyline Plot method suggests fast population growth about 6500 years ago, consistent with the time of the establishment of the Baltic population inferred from the distribution of radiocarbon dated seal bones. The analysis of phylogenetic relationships between the extinct Baltic harp seals and extant harp seals from the North Atlantic showed that the Baltic population was established by a large and diverse founder population. The pattern of haplotype sharing suggests that the founder population most likely originated from the White Sea breeding colony, which is spatially closest. The reconstruction of the harp seal population dynamics also suggests that this population declined abruptly about 1000 years ago, which coincided with the Medieval Warm Period (AD 950-1250).
Nucleotide diversity of the ancient harp seals in mtDNA control region was comparable with the ancient ringed seals (the most numerous seal species in the Baltic at present) and higher than grey seals and harbour seals. This suggests that the harp seal population declined from numbers comparable with the most numerous seal species in the Baltic Sea to extinction within a period of several hundred years. Possible causes of such decline include climate-related environmental change, overhunting, competition with other seal species, and inbreeding due to genetic isolation. Our results allow us to exclude the last potential cause, as genetic diversity of harp seal in the small Baltic Sea basin was higher than in two Northwest Atlantic breeding colonies, while the population numbers in the entire Northwest Atlantic were estimated at 4.5 million. Climate-related environmental change could have caused the extinction of this ice-breeding species, as the Baltic Sea was the southernmost part of its range. However, throughout its history this population survived warmer temperatures than in the time of its extinction, so climate warming is unlikely to be the main cause of the extinction. However, the decline of the harp seal population also coincided with the decline in the salinity of the Baltic Sea, which implies the decline in sea productivity. This could have intensified competition for food resources with other seal species, as well as with humans. Competition with another seal species would have resulted in population growth of these species after the harp seal extinction. Indeed, the grey seal shows a strong signal of population growth about 500 years ago, while the last known record of the harp seal dates for about 700 years ago. Therefore, it is likely that competition with the grey seal contributed to the harp seal extinction. The effect of hunting by humans is more difficult to assess. However, widespread presence of harp seals in archaeological record (Storå and Ericson 2004) combined with the significant increase in human population size in the Baltic Sea region during the Medieval Warm Period (Tallavaara and Seppa 2012) suggest that hunting could have contributed to the harp seal extinction.
Our research also provides the first data on the genetic variability of ancient (13710- 2900 years before present) and historical, pre-bottleneck populations (from the period 1843-1990) of each of the three extant seal species, and reconstruction of effective population sizes. The ringed seal had consistently highest and the harbour seal lowest effective size. Our results also suggest extensive gene flow among different regions of the Baltic Sea, as well as between the Baltic and Skagerrak/Kattegat straits. The reconstruction of Holocene population dynamics for the ringed seal and harbour seal suggests population growth throughout the entire period studied, until modern times. The same reconstruction for the grey seal suggests low effective population size until about 500 years ago, when a sudden population growth was observed, followed by a decline in the XX century. The comparison of modern pre-bottleneck and post-bottleneck populations showed a decline in haplotype diversity in each extant species.
Conclusions
The reconstruction of the demographic changes in the Baltic harp seal population suggests that it had high effective size throughout most of its history, and declined abruptly towards extinction. Although this decline coincided with the Medieval Warm Period, climate warming is unlikely to be the major cause of the extinction, as no effects of earlier periods of climate warming were reflected in the population dynamics. We also did not find any clear effects of climatic fluctuations on population dynamics of other seal species. The Baltic seals, including two exclusively ice-breeding species (the harp seal and the ringed seal) seem to be surprisingly resilient to climate-induced environmental change. In contrast, the recent severe population decline in all three extant species showed that they are vulnerable to hunting, and it is likely that overhunting contributed to the harp seal extinction. Moreover, the comparison of population dynamics patterns in the four Baltic seal species suggest that the harp seal extinction could have been partially caused by competition with the grey seal, which was likely intensified by a decline in sea salinity and a resulting decline in sea productivity.
Potential applications and impact
The results of this project contribute to a better understanding of the processes underlying population extinction or survival, which is a fundamental question of evolutionary biology with very important practical implications for biodiversity conservation. Besides contributing to the general knowledge in the area of evolutionary and conservation biology, this project can be also applied to a particular case of conservation of seals in the Baltic Sea. Our results suggest that climate change was not a major driver of population dynamics of Baltic seals, including the two exclusively ice-breeding species, which has important conservation implications. The knowledge obtained in this project may be applied towards the development of predictive models on the impact of on-going human activities (including culling) and climate change on the Baltic seals, which will help to develop effective strategies for their conservation. This will contribute to the implementation of the European Union's Marine Strategy and the Baltic Sea Action Plan of the Helsinki Commission.
References
Storå J, Ericson PGP (2004) A prehistoric breeding population of harp seals (Phoca groenlandica) in the Baltic Sea. Mar. Mamm. Sci. 20: 115-133.
Tallavaara M, Seppa H (2012) Did the mid-Holocene environmental changes cause the boom and bust of hunter-gatherer population size in eastern Fennoscandia? The Holocene 22: 215225.