The challenges of detecting subtle population structure and its importance for the conservation of emperor penguins

Abstract

Understanding the boundaries of breeding populations is of great importance for conservation efforts and estimates of extinction risk for threatened species. However, determining these boundaries can be difficult when population structure is subtle. Emperor penguins are highly reliant on sea ice, and some populations may be in jeopardy as climate change alters sea-ice extent and quality. An understanding of emperor penguin population structure is therefore urgently needed. Two previous studies have differed in their conclusions, particularly whether the Ross Sea, a major stronghold for the species, is isolated or not. We assessed emperor penguin population structure using 4,596 genome-wide single nucleotide polymorphisms (SNPs), characterized in 110 individuals (10-16 per colony) from eight colonies around Antarctica. In contrast to a previous conclusion that emperor penguins are panmictic around the entire continent, we find that emperor penguins comprise at least four metapopulations, and that the Ross Sea is clearly a distinct metapopulation. Using larger sample sizes and a thorough assessment of the limitations of different analytical methods, we have shown that population structure within emperor penguins does exist and argue that its recognition is vital for the effective conservation of the species. We discuss the many difficulties that molecular ecologists and managers face in the detection and interpretation of subtle population structure using large SNP data sets, and argue that subtle structure should be taken into account when determining management strategies for threatened species, until accurate estimates of demographic connectivity among populations can be made.

Genomics detects population structure within and between ocean basins in a circumpolar seabird: The white‐chinned petrel

“…The island‐level resolution of our data, which included genetics of previously unsampled populations (Campbell, Falkland and Kerguelen islands), provides comprehensive information for guiding conservation priorities, management and policy. Our work also adds to a growing number of studies on Southern Ocean taxa that have revealed more differentiation using genomic data sets than that detected with traditional approaches (Clucas et al, ; Fraser, McGaughran, Chuah, & Waters, ; Piertney et al, ; Trucchi et al, ; Younger et al, , ). This highlights the possibility of important but undetected structuring in other wide‐ranging Southern Ocean species.…”

“…Despite more comprehensive sampling, our cyt b results were very similar to those for cyt b in Techow et al (2009), suggesting that the newly-detected multi-region structure was based on the temporal resolution of markers and not increased sampling. A growing number of studies on Southern Ocean taxa show previously suspected fine-scale population structure using GBS data in species ranging from Durvillaea kelp and brown rats Rattus norvegicus, to emperor and king penguins (Fraser et al, 2016;Fraser et al, 2018;Piertney et al, 2016;Younger et al, 2017Younger et al, , 2015; but see Clucas et al, 2016;Trucchi et al, 2014). In the case of white-chinned petrels, the finer-scale multi-region structure identified using GBS data is consistent with tracking and isotopic work which shows that birds from these regions differ in foraging habitat or at-sea distribution, particularly during the nonbreeding period (Catard et al, 2000;Jaeger et al, 2013;Phillips et al, 2006;Rexer-Huber, 2017;Rollinson et al, 2018).…”

Comparative population genomics reveals key barriers to dispersal in Southern Ocean penguins

“…Among the eight sampled emperor penguin colonies (Figure b), there are four genetically differentiated metapopulations (Younger et al., ). The Ross Sea metapopulation appears the most divergent from the rest, consistent with findings from mitochondrial DNA (Younger, Clucas, et al., ).…”

“…Banding studies initially suggested a high degree of philopatry in many species (Weimerskirch, Jouventin, Mougin, Stahl, & Van, ), and, until recently (Jenouvrier, Garnier, Patout, & Desvillettes, ), forecasts of extinction risk had not considered the potential buffering effect of dispersal (Cimino, Lynch, Saba, & Oliver, ; Jenouvrier et al., ). Genetic analyses (Clucas, Younger et al., ; Freer et al., ; Roeder et al., ; Younger, Clucas, et al., , ), observations of colony movements (LaRue, Kooyman, Lynch, & Fretwell, ) and fluctuations in colony size (Kooyman & Ponganis, ) indicate that dispersal may be common. However, hydrographic features are thought to act as barriers to dispersal in a handful of sub‐Antarctic and temperate penguin species (see Munro & Burg, , for a review).…”

The Paris Agreement objectives will likely halt future declines of emperor penguins

“…This counterintuitive result occurs because dispersal allows poor quality habitats that would otherwise be sequestered to function as connected demographic sinks that rapidly deplete the entire metapopulation (Jenouvrier et al, ). The adaptive capacity of emperor penguins is unknown, but is likely limited because they have a long life spans, delayed maturity, and low reproductive rates, coupled with low genetic diversity (Younger et al, ). The biological capacity for emperor penguins to ‘cope’ with climate change through adaptation or dispersal to suitable habitats is therefore likely to be minimal (but see Younger et al, ).…”