Shallow population histories in deep evolutionary lineages of marine fishes: insights from sardines and anchovies and lessons for conservation

Abstract

Most surveys of mitochondrial DNA (mtDNA) in marine fishes reveal low levels of sequence divergence between haplotypes relative to the differentiation observed between sister taxa. It is unclear whether this pattern is due to rapid lineage sorting accelerated by sweepstakes recruitment, historical bottlenecks in population size, founder events, or natural selection, any of which could retard the accumulation of deep mtDNA lineages. Recent advances in paleoclimate research prompt a reexamination of oceanographic processes as a fundamental influence on genetic diversity; evidence from ice cores and anaerobic marine sediments document strong regime shifts in the world's oceans in concert with periodic climatic changes. These changes in sea surface temperatures, current pathways, upwelling intensities, and retention eddies are likely harbingers of severe fluctuations in population size or regional extinctions. Sardines (Sardina, Sardinops) and anchovies (Engraulis) are used to assess the consequences of such oceanographic processes on marine fish intrageneric gene genealogies. Representatives of these two groups occur in temperate boundary currents on a global scale, and these regional populations are known to fluctuate markedly. Biogeographic and genetic data indicate that Sardinops has persisted for at least 20 million years, yet the mtDNA genealogy for this group coalesces in less than half a million years and points to a recent founding of populations around the rim of the Indian-Pacific Ocean. Phylogeographic analysis of Old World anchovies reveals a Pleistocene dispersal from the Pacific to the Atlantic, almost certainly via southern Africa, followed by a very recent recolonization from Europe to southern Africa. These results demonstrate that regional populations of sardines and anchovies are subject to periodic extinctions and recolonizations. Such climate-associated dynamics may explain the low levels of nucleotide diversity and the shallow coalescence of mtDNA genealogies. If these findings apply generally to marine fishes, management strategies should incorporate the idea that even extremely abundant populations may be relatively fragile on ecological and evolutionary time scales.