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Climate change selects for heterozygosity in a declining fur seal population

Nature volume 511, pages 462–465 (2014)Cite this article

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Abstract

Global environmental change is expected to alter selection pressures in many biological systems1,2,3, but the long-term molecular and life history data required to quantify changes in selection are rare4. An unusual opportunity is afforded by three decades of individual-based data collected from a declining population of Antarctic fur seals in the South Atlantic. Here, climate change has reduced prey availability and caused a significant decline in seal birth weight. However, the mean age and size of females recruiting into the breeding population are increasing. We show that such females have significantly higher heterozygosity (a measure of within-individual genetic variation) than their non-recruiting siblings and their own mothers. Thus, breeding female heterozygosity has increased by 8.5% per generation over the last two decades. Nonetheless, as heterozygosity is not inherited from mothers to daughters, substantial heterozygote advantage is not transmitted from one generation to the next and the decreasing viability of homozygous individuals causes the population to decline. Our results provide compelling evidence that selection due to climate change is intensifying, with far-reaching consequences for demography as well as phenotypic and genetic variation.

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Figure 1: Long-term population and phenotypic change associated with the Southern Annular Mode (SAM) in females of an Antarctic fur seal population.
Figure 2: Long-term trend in breeding female homozygosity, expressed as homozygosity weighted by locus (HL), and the effects of homozygosity on female recruitment and breeding success.
Figure 3: Strength of viability selection on homozygosity weighted by locus (HL) for the period 2002–12 inclusive.

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Acknowledgements

The authors thank the many fieldworkers who have contributed to data collection over the years. We are also grateful to W. Amos, J. Bascompte, M. Boerner, K. Dasmahapatra, O. Krüger and I. Staniland for advice and feedback on the manuscript, together with T. Coulson for helpful referee comments. This work contributes to the Long Term Monitoring and Survey project and Ecosystems project of the British Antarctic Survey, Natural Environment Research Council, part of the Polar Science for Planet Earth programme. The genetic work was supported by a Marie Curie FP7-Reintegration-Grant within the 7th European Community Framework Programme (PCIG-GA-2011-303618) and a Deutsche Forschungsgemeinschaft standard grant (HO 5122/3-1) awarded to J.I.H.

Author information

Authors and Affiliations

  1. British Antarctic Survey, Natural Environment Research Council, High Cross, Madingley Road, Cambridge CB3 0ET, UK,

    Jaume Forcada

  2. Department of Animal Behaviour, University of Bielefeld, Postfach 100131, 33501 Bielefeld, Germany,

    Joseph Ivan Hoffman

Authors
  1. Jaume Forcada
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  2. Joseph Ivan Hoffman
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Contributions

J.F. conceived, designed and conducted the biometric, mark–recapture, demographic and population modelling and subsequent phenotypic and evolutionary demographic analysis; J.I.H. generated and analysed the genetic data. The authors jointly interpreted the results and wrote the manuscript.

Corresponding author

Correspondence to Jaume Forcada.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 Antarctic fur seal life cycle and directed acyclic graph of multi-event mark–recapture models used to estimate vital rates.

a, In the life cycle graph, nodes correspond to stages and arrows to probabilities of transition () between stages (Supplementary Information), from year t to t + 1. Subscripts are for ages 0, for weanlings, to 6 at full physical maturity, and breeding stages. P6 acts as a terminal node for individuals observed alive but never recruited. Fertilities (f) are female weanlings contributed by females breeding at t + 1. b, The acyclic graph shows intermediate sets of stages which are connected by rows, with each stage in a row being represented by a node. Different transitions are represented by arrows linking intermediate states. Nodes are different in a and b. See Supplementary Information for definitions of stages and vital rates.

Extended Data Figure 2 Variation in survival probability and breeding propensity (fecundity) with variation in the SAM index.

Panel a shows survival of first-year pre-breeders in red, including its variation with homozygosity weighted by locus (HL); averaged survival for years 1 to 6 is shown in blue. Panel b shows age-specific survival for recruiting seals, and panel c the survival for adults (that is, seals with previous breeding experience) with variation by stages defined according to previous breeding outcomes (successful, failed, or deferred breeding). Panel d shows inter-annual breeding propensity for recently recruited seals and for experienced breeders. All vertical bars show 95% CIs.

Extended Data Figure 3 Sensitivity of the population growth rate (log(λ)) to changes in statistical parameters of vital rates describing the survival and fertility functions in integral projection models.

Panels a–c show sensitivity to survival of first year females (a), females of ages 1 to 7 (b; continuous lines for pre-breeders and dashed for breeders), and ages 8 or above (c). Panel d shows sensitivity to recruitment (α) and panel e shows sensitivity to inheritance (H(h′|h)), with a dashed line for the variance intercept. Panels f and g show sensitivity to fecundity for ages 3 to 7, and 8 or above, respectively. Panels h and i show sensitivities to breeding success (ς) for ages 3 to 7, and 8 or above, respectively. Red lines are intercepts, black and grey are linear and quadratic SAM index effects, green are homozygosity weighted by locus (HL) effects, and blue are linear age effects. The scale of the vertical axes in panels a–c and e are an order of magnitude higher than in the other panels.

Extended Data Figure 4 Sensitivity of the mean population homozygosity weighted by locus () to changes in statistical parameters of the vital rates describing the survival and fertility functions in integral projection models.

Panels a–d show sensitivity to survival of first year females (a), pre-breeders of ages 1 to 7 (b), breeders aged 8 or above (c), and breeders of ages 3 to 7 (d). Panel e shows sensitivity to recruitment (α), and panels f and g show sensitivity to fecundity for ages 3 to 7, and ages 8 or above, respectively. Panel h shows sensitivity to inheritance (H(h′|h)), where the dashed line indicates the variance parameter. Panels i and j show sensitivity to breeding success for ages 3 to 7, and ages 8 or above, respectively. Colours are red for intercept, black and grey for linear and quadratic SAM index effects, respectively, green for HL effects, and blue for linear age effects.

Extended Data Figure 5 Sensitivity of the strength of viability selection (VS) on homozygosity weighted by locus (HL) to statistical parameters of vital rates describing the survival and fertility functions of integrated projection models.

Panels a–d show sensitivity to survival of first-year females (a), pre-breeders of ages 1 to 7 (b), breeders of ages 3 to 7 (c) and breeders of ages 8 or above (d). Panel e shows sensitivity to recruitment (α) and panels f and g show sensitivity to fecundity for ages 3 to 7, and 8 or above, respectively. Panel h shows the sensitivity to inheritance (H(h′|h)), where the dashed line is for the variance parameter. Panels i and j show sensitivities to breeding success for ages 3 to 7, and ages 8 or above, respectively. Colours are red for intercept, black and grey for linear and quadratic SAM index effects, respectively, green for HL effects, and dark blue and light blue for linear and quadratic age effects, respectively. Note that the scale of the vertical axis in panel a is an order of magnitude larger than the other panels.

Extended Data Figure 6 Long-term trend in breeding female homozygosity decomposed by locus.

Coloured lines show mean annual homozygosity weighted by locus (HL) values for each of the loci exhibiting significant declining trends (see also Extended Data Table 3). The equivalent relationship for multilocus HL is shown below for reference, with the shaded area representing the 95% confidence interval of a fitted linear model of HL against year, and the vertical bars representing 95% confidence limits of the annual estimates.

Extended Data Table 1 Selection of multi-event mark-recapture models of Antarctic fur seal females at Bird Island based on QAICc (see Methods in the Supplementary Information)
Full size table
Extended Data Table 2 Sensitivity analysis and retrospective contribution of Antarctic fur seal vital rates to λ
Full size table
Extended Data Table 3 Long-term trends in heterozygosity decomposed by locus
Full size table

Supplementary information

Supplementary Information

This file contains Supplementary Methods and additional references. (PDF 403 kb)

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Forcada, J., Hoffman, J. Climate change selects for heterozygosity in a declining fur seal population. Nature 511, 462–465 (2014). https://doi.org/10.1038/nature13542

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