Shallow Population Histories in Deep Evolutionary Lineages of Marine Fishes: Insights From Sardines and Anchovies and Lessons for Conservation W. S. Grant and B. W. Bowen Most surveys of mitochondrial DNA (mtDNA) in marine ®shes 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 re- examination of oceanographic processes as a fundamental in¯uence 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 ¯uctuations in pop- ulation size or regional extinctions. Sardines (Sardina, Sardinops) and anchovies (Engraulis) are used to assess the consequences of such oceanographic process- es on marine ®sh intrageneric gene genealogies. Representatives of these two groups occur in temperate boundary currents on a global scale, and these regional populations are known to ¯uctuate markedly. Biogeographic and genetic data in- dicate 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±Paci®c Ocean. Phy- logeographic analysis of Old World anchovies reveals a Pleistocene dispersal from the Paci®c 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 extinc- tions and recolonizations. Such climate-associated dynamics may explain the low levels of nucleotide diversity and the shallow coalescence of mtDNA genealogies. If these ®ndings apply generally to marine ®shes, management strategies should incorporate the idea that even extremely abundant populations may be relatively fragile on ecological and evolutionary time scales. From the Conservation Biology Division, Northwest Fisheries Science Center, NOAA, Seattle, Washington, and the Department of Fisheries and Aquatic Sciences, A recurring debate in evolutionary biology roki 1997). Although several early hypoth- University of Florida, Gainesville, Florida. We thank A. is over the extent to which microevolution- eses about population regulation are now Bass, A. Clark, and A. Garcia for technical support, and ary processes operating within a species can R. Leslie and A. Payne (Sea Fisheries Research Insti- be extrapolated to explain macroevolution- discounted on the basis of ®eld studies, tute, Cape Town, South Africa), T. Kobayashi (National ary differences among species . other hypotheses remain untested be- Research Institute of Fisheries Science, Yokohama, Ja- Avise et al. (1987, p. 489) pan), S. Jablanski (SUDEPPE, Rio de Janeiro, Brazil), cause of the lack of an appropriate tool. and J. Shaklee (CSIRO, Canberra, Australia) for gener- Recent advances in sampling technology ously providing samples for the various studies re- and satellite imagery show considerable viewed in this article. K. Bailey, J. Gold, S. Karl, T. To understand the dynamics of marine Streelman, F. Utter, and R. Waples provided insightful ®sh populations, researchers must identi- promise, demonstrating, for example, that comments on the manuscript. Genetic studies of sar- fy the conditions that regulate reproduc- in the California Current egg and larval dines and anchovies were supported by the U.S. Na- tional Science Foundation and by the Foundation for tion, population growth, and persistence. production is contingent on small upwell- Research Development, Pretoria, South Africa. Address On short (ecological) time scales, a vari- ing plumes along the coast (Lo et al. correspondence to Dr. Grant, Northwest Fisheries Sci- 1996). ence Center, 2725 Montlake Boulevard East, Seattle, WA ety of factors, including nutrient cycles, 98112-2097, or e-mail: [email protected]. This paper food-chain processes, spawning, preda- One emerging generalization from mo- was delivered at a symposium entitled ``Conservation tion, recruitment, and climate have been lecular analyses is that marine ®shes are and Genetics of Marine Organisms'' sponsored by the American Genetics Association at the University of Vic- proposed as primary regulators of abun- often characterized by shallow population toria, Victoria, BC, Canada, June 7, 1997. dance (Butler 1991; Parrish and Mallicoate genetic architectures, even though genetic q 1998 The American Genetic Association 89:415±426 1995; Smith et al. 1992; Watanabe and Ku- divergence from sister taxa indicates sep- 415 arations of millions of years. In a review of mitochondrial DNA (mtDNA) diversity in widely distributed marine ®shes, Shields and Gust (1995) noted a recurring pattern of a single or a few prevalent haplotypes with numerous rare haplotypes that were one or two mutations removed from the common haplotype. These starlike phylog- enies characterize regional populations of haddock (Melanogrammus aegle®nus; Zwa- nenburg et al. 1992), Atlantic cod (Gadus morhua; Carr and Marshall 1991; Smith et al. 1989), cape hake (Merluccius capensis; Becker et al. 1988), deepwater hake (M. paradoxus; Becker et al. 1988), Atlantic herring (Clupea harengus; Korn®eld and Bogdanowicz 1987), Paci®c herring (C. pal- lasi; Schweigert and Withler 1990), red drum (Sciaenops ocellatus; Gold et al. 1993), black drum (Pogonias cromis; Gold et al. 1994), greater amberjack (Seriola du- merili; Richardson and Gold 1993), red snapper (Lutjanus compechanus; Camper et al. 1993), Spanish sardine (Sardinella au- rita; Tringali and Wilson 1993), orange roughy (Hoplostethus atlanticus; Baker et al. 1995; Ovenden et al. 1989; Smolenski et al. 1993), Atlantic capelin (Mallotus villo- sus; Dodson et al. 1991), albacore tuna (Thunnus alalunga; Graves and Dizon 1989), and skipjack tuna (Katsuwonus pe- lamis; Graves et al. 1984). Shallow haplo- type divergences atop long lineages are Figure 1. Geographical distributions of sardines (Sardina, Sardinops) and anchovies (Engraulis) with 138C and also clearly illustrated in Figures 4 and 5 258C isotherms (dashed lines). of Bermingham et al. (1997) for species of damsel®sh isolated about 3 million years ago by the formation of the Panama isth- boundary current systems, and because colonizations), founder events, dispersals, mus. Explanations for this widespread pat- regional populations of both groups show and divergence between isolated popula- tern include a large variance in reproduc- strong ¯uctuations in abundance that tions. These case histories are used to tive success that leads to the propagation have been attributed to high levels of ex- evaluate the hypotheses that have been of only a few haplotypes (Shields and Gust ploitation (Murphy 1966, 1967). For ex- forwarded to explain shallow gene gene- 1995), overharvesting (Camper et al. ample, the biomass of sardines (Sardinops alogies in other marine ®shes. The forces 1993), the physical nature of the pelagic caeruleus) in the California Current peaked that attenuate mtDNA diversity may be a realm (Graves 1995), recent habitat reduc- at an estimated 3,600,000 metric tons key to understanding population regula- tions (Shulman and Bermingham 1995), (MT) in the 1930s (Murphy 1966) then de- tion in marine ®shes. Hence these shallow population bottlenecks (Gold et al. 1994), clined during a period of intensive har- intraspeci®c phylogenies carry implica- or other ``demographic events'' (Dodson vests to about 5,000±6,000 MT in 1975 tions for microevolution and marine bio- et al. 1991). (Barnes et al. 1992; Wolf 1992). The bio- geography as well as resource manage- This phenomenon is also apparent in mass of California anchovies (Engraulis ment in the face of climatic change and sardines (Sardina, Sardinops) and ancho- mordax) has also ¯uctuated from lows in high exploitation (Hansen et al. 1981; San- vies (Engraulis). Both groups are globally the 1950s to a high in the 1970s (Lo and ter et al. 1996). distributed in temperate zones and have Methot 1989). All of the regional popula- representative species or populations in tions of sardines and anchovies have sim- Long-Term Climatic Variability and most of the world's temperate boundary ilar histories of declines and partial recov- Population Abundance Cycles current systems (Figure 1). These popu- eries which are attributed to harvests or lations are isolated by vast expanses of to climatic and oceanographic changes It is widely accepted that climatic changes open ocean or by warm tropical waters (Lluch-Belda et al. 1989). are capable of limiting abundances, but that restrict movement across the equa- Here we review genetic evidence from the impact of these changes on marine tor. Sardines and anchovies are a peren- allozyme and mtDNA datasets for sardines biodiversity has only recently been appre- nial concern to marine resource managers and anchovies that may bear imprints of ciated (Hayward 1997; Roemmich and because they represent the majority of the population collapses (bottlenecks), meta- McGowan 1995; Watson et al. 1996). Rapid