oa Whale shark genetics: Where are we now and where should we be going?

Background Classic ecological approaches can reveal only glimpses of the behavioral spectrum of a longlived migratory species. Genetic analysis has the potential to inform the migratory behavior and reproductive habits of animals that are difficult or impossible to observe in the wild. Although studied primarily as juveniles at seasonal feeding aggregations, whale sharks are believed to be capable of extensive migrations. The frequency and magnitude of these movements is unknown, as is the degree to which they mediate gene flow between populations. Recent studies have asked whether the sharks observed at different aggregation sites show evidence of genetic structure, or whether they constitute a single breeding population. We published a preliminary study in 2009, based on microsatellite analysis of animals from numerous globally distributed aggregation sites, with a finding of minimal genetic differentiation. Approach Our genetic study is ongoing, and now encompasses hundreds of whale sharks representing all major aggregations worldwide. Other groups have also performed genetic analyses of whale shark population structure, focusing on both regional and global scales. Particularly for studies using microsatellite markers, direct comparisons across laboratories and platforms are not possible. Synthesizing the overall conclusions from aggregate genetic studies, however, provides additional power to understand species behaviors. Results Initial analysis of broadly distributed whale sharks found only low levels of genetic differentiation across geographically distinct populations. While sharks from the Western Atlantic Ocean showed slightly greater differentiation from Pacific/Indian Ocean animals than these populations did from each other, this result was not statistically significant. An expanded data set has now provided stronger analytical resolution between populations, revealing subtle yet statistically significant levels of genetic differentiation of Atlantic sharks. Conclusions Our previous analysis suggested gene flow between whale shark populations at a level sufficient to normalize genetic differentiation. Combined with satellite tracking and other data, these results confirmed that whale sharks can and do migrate between oceans. An expanded study, however, along with data published by other groups, now indicates reduced mixing between Western Atlantic and Indian/Pacific sharks. A significant body of evidence therefore indicates that whale sharks do not have strong population structure, nor do they represent a single panmictic population. Rather they occupy a more biologically realistic intermediate, with varying degrees of isolation by distance and by ecological features. Future genetic characterization should focus on the addition of yet unstudied whale shark populations, on building a robust mitochondrial haplotype dataset with broad applicability, and on technical standardization that could allow comparisons between microsatellite data sets across laboratories and platforms.