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The Evolutionary Impact of Invasive Species

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The Evolutionary Impact of Invasive Species Colloquium The evolutionary impact of invasive species H. A. Mooney* and E. E. Cleland Department of Biological Sciences, Stanford University, Stanford, CA 94305-5020 Since the Age of Exploration began, there has been a drastic and biotic environments that exist now are quite different from breaching of biogeographic barriers that previously had isolated those that have existed in recent geological times. the continental biotas for millions of years. We explore the International commerce has facilitated the movement of nature of these recent biotic exchanges and their consequences species; this is true globally and across taxonomic groups. on evolutionary processes. The direct evidence of evolutionary Ironically, this has increased species richness in many places consequences of the biotic rearrangements is of variable quality, where new species are introduced. The actual numbers of but the results of trajectories are becoming clear as the number individuals and species being transported across biogeographical of studies increases. There are examples of invasive species barriers every day is presumably enormous. However, only a altering the evolutionary pathway of native species by compet- small fraction of those transported species become established, itive exclusion, niche displacement, hybridization, introgression, and of these generally only about 1% become pests (5). Over predation, and ultimately extinction. Invaders themselves time however, these additions have become substantial. There evolve in response to their interactions with natives, as well as are now as many alien established plant species in New Zealand in response to the new abiotic environment. Flexibility in be- as there are native species. Many countries have 20% or more havior, and mutualistic interactions, can aid in the success of alien species in their floras (6). There are few geographic invaders in their new environment. generalities to these trends; the strongest is that islands, in particular, have been the recipients of the largest proportional numbers of invaders. Biotic homogenization within continents is he Nature of the Problem. Those of us alive today are witness- equally as striking as mixing among oceans. As one example, Ting the consequences a number of truly grand, but un- Rahel (7) notes that in the United States pairs of states on planned, biological experiments. They are the result of the average now share 15 more species than they did before Euro- activities of a massive human population that is still growing and pean settlement. The states of Arizona and Montana, which increasing its impact on the Earth. Because there are no controls previously had no fish species in common, now share 33 species on these experiments, as such, we must look to biological in their faunas. patterns through time for perspective on the consequences of the Mack (8) estimates that over the last 500 years, invasive species mixing of biotas. This is a challenge because environments of the have come to dominate 3% of the Earth’s ice-free surface. Vast past also changed, sometimes abruptly. land or waterscapes, in certain regions, are completely domi- These historical fluctuations in climate and biota of the past nated by alien species, such as the star thistle Centaurea solstitialis have led some to say that nothing new is happening that has not in the rangelands of California, cheatgrass (Bromus tectorum)in already happened before. The response to this proposition is yes, the intermountain regions of the western United States, and but the rate of change in the composition of the atmosphere today water hyacinth (Eichornia crassipes) in many tropical lakes and exceeds anything of the past, as will the consequent rate of rivers. climate change. This is also true to a large degree in the extent of migration of species among continents. Before the Age of The Rates of Exchange. As the volume of global trade increases, Exploration, dispersal of organisms across these great biogeo- one would expect the rate of establishment of alien species to graphic barriers was a low-probability event; however, today this increase also; data support this prediction. Cohen and Carlton is routine. In this paper we briefly summarize the consequences (9) noted that the rate of invasion into San Francisco Bay has of the massive movement of organisms across these barriers in increased from approximately one new invader per year in the terms of the course of future evolution. period of 1851–1960, to more than three new invaders per year We start this essay with two quotes providing perspectives on in the period of 1961–1995. In the United States the numbers of the problem. One is from the pioneering work of Charles Elton fish introductions, either from foreign sources or across water- (1), who stated, ‘‘We must make no mistake: we are seeing one shed boundaries, has increased dramatically. In the period of the great historical convulsions in the world’s fauna and between 1850 and 1900, 67 species were introduced, between flora.’’ Elton certainly had no doubts of the magnitude of the 1901 and 1950, 140 species, and between 1951 and 1996, 488 invasive species issue. More recently, Geerat Vermeij (2) re- species (ref. 10 and the web site referred to therein). marked specifically about the evolutionary consequences of this In addition to the greater number of species crossing borders convulsion, ‘‘. if newcomers arrive from far away as the result there is also a buildup in the invasive potential of those nonnative species already established in a region, as immigration increases of large-scale alterations in geography or climate, the change in their population sizes. ‘‘Introduced species’’ may stay at a fairly selective regime and the evolutionary responses to this change low population size for years and then explode at some later could be dramatic.’’ We examine here some of the evidence for date—the so-called lag effect. This lag effect may simply be the this potentially dramatic scenario. result of the normal increase in size and distribution of a population. For instance, Bromus tectorum was introduced to The Changing Evolutionary Landscape. It is commonly acknowl- edged that the abiotic environment is being greatly altered because of massive land-use alteration and emerging climate This paper was presented at the National Academy of Sciences colloquium, ‘‘The Future of change (3, 4). However, an equally drastic alteration is occurring Evolution,’’ held March 16–20, 2000, at the Arnold and Mabel Beckman Center in Irvine, CA. in the composition of biotic communities. The kinds of physical *To whom reprint requests should be addressed. E-mail: [email protected]. 5446–5451 ͉ PNAS ͉ May 8, 2001 ͉ vol. 98 ͉ no. 10 www.pnas.org͞cgi͞doi͞10.1073͞pnas.091093398 Downloaded by guest on October 2, 2021 intermountain western North America around 1890, and re- The Direct Evolutionary Consequences of Mixing mained in localized populations for 20 years. This lag phase was Evolutionary Adjustments of Invaders and of the Invaded. We turn to followed by 20 years of logistic range expansion; by 1930 B. contemporary studies to give us some indication of the evolu- 2 tectorum was dominant over 200,000 km (11). tionary impact of invasive species. Recent studies have shown Crooks and Soule (12) note that in addition to the normal that invaders can rapidly adapt to the new environments in which population growth lag phase there are other mechanisms that they find themselves. Huey et al. (18) demonstrated how an can keep newly introduced species at low levels for decades introduction of a new fruit fly into the west coast of North before they become invasive. These include environmental America resulted in the evolution, in only 20 years, of an change, both biotic and abiotic, after establishment and genetic apparently adaptive cline related to wing size, throughout the changes to the founder populations that enable subsequent vast new latitudinal range extending from southern California to spread. Evidence for the former cases is abundant but scarce for British Columbia. The cline that developed in North American the latter. female flies was similar to that found in the European native In summary, the biotic background for evolution has been populations. Interestingly, the developmental basis for the cline changing since the Age of Exploration, and at an ever- of wing size was different in Europe than for the invader in North accelerating pace because of accumulative effects of the num- America, although the functional result was the same, providing bers of species involved, the increased rate of exchange, and the additional evidence for the adaptive advantage of this set of lag debts that communities have amassed. traits. Drosphilia subobscura were introduced into North America in Looking to the Past. There are examples from the past of sudden 1982; shortly thereafter Ayala et al. (19) described the invasion mixing of biotas that were formerly isolated; one of these is fairly as ‘‘a grand experiment in evolution.’’ This was certainly an recent and instructive. The biota from the Red Sea and the accurate prediction, given the results of Huey et al. 10 years later, Mediterranean Sea were reconnected, after a separation of and only 20 years after the beginning of the invasion event. millions of years, by the construction of the Suez Canal in 1869. There are other documented instances of an invading species The pathway for movement between these water bodies has adapting to its new environment. For example, Johnston and changed since 1869 because of the varying salinity of a lake in the Selander (20) described the evolution of apparently adaptive canal system; that is, there has not been totally free exchange clines in body size and feather color in English sparrows that without barriers. Nonetheless, over 250 species, 34 new genera, were introduced into North America in 1852 and that subse- and 13 new families have moved into the Mediterranean Sea quently established a large geographical range.
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