Many taxa of marine animals have increased in size through time, with some of the largest that have ever existed being vertebrate filter-feeders targeting plankton. Present day ecological studies show that the size and body structure of whale sharks is likely to reflect a strategy for gigantothermy that conserves heat while foraging in cool deep waters. However, the temperature of the oceans has changed through time, as has the composition of the guild of large, filterfeeding fishes. What do these changes reveal about the evolution and ecology of whale sharks? I synthesise the results of new analyses of the fossils of filter-feeding fishes that were the largest representatives of their guild over the last 160 million years with ecological studies of whale sharks and filter-feeding whales. This analysis offers an opportunity to examine the evolutionary forces that have shaped the biology of whale sharks. Throughout time, bony fishes, sharks and whales that were obligate ram filter-feeders attained similar maximum lengths of around 16–20 m and in the case of the whale shark, body masses equal to, or even greater than, many baleen whales today. This shows that ecological niche and mode of feeding are more important drivers of limits to the body size of fishes than phylogeny. The relatively small variation in maximum sizes of the largest ram filter-feeders over the last 165 million years suggests that animals within this guild will not continue to increase insize through evolutionary time, but have already attained sizes constrained by their environment and mode of feeding.


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