Journal of Animal Ecology (1987), 56, 1-9 CAUSES OF ECOLOGICAL SUCCESS: THE CASE OF THE ANTS. THE SIXTH TANSLEY LECTURE* BY EDWARD 0. WILSON Museum of ComparativeZoology, Harvard University, Cambridge,Massachusetts 02138, U.S.A. INTRODUCTION The key remaining questions of evolutionary biology are more ecological than genetic in nature. In spite of the continuing great vitality of genetics in general, the known mechanisms of heredity appear to be sufficient to explain the observed phenomena of evolution. This is not to say that all processes of genetic change have been discovered. It may even prove true that extragenetic constraints on embryonic development, such as fundamental physical limits on cell size and configuration, play a role in evolution. What I am suggesting instead is that nothing empirically known at the present time about the nature and rate of evolution even hints at the existence of undiscovered hereditary processes. Consequently, what we know for sure that we do not know is largely ecological in nature. And ecologically-based problems of basic importance abound. One of the more obvious is why there are a certain number of species on Earth and not some other, in particular why 10 million (if that, say, proves to be the number) and not a thousand or a hundred million. Another unanswered question is why certain groups of organisms speciate profusely and spread over the world while otherwise similar ones remain undiversified and static. And that leads ineluctably to a third, related question, the meaning of ecological success. The subject has received remarkably little attention, perhaps because it is difficult to express with any precision and may appear to be more semantic than scientific. To take an example on which all can hopefully agree, we intuitively think of the ants as a successful group. Can success be usefully defined in such organisms? And if so, which if any evolutionary strategies consistently confer it? WHAT IS ECOLOGICAL SUCCESS? The principal force impelling evolution, natural selection, is simply all the events that cause differential survival and reproduction. It seems intuitively right and indeed can be defended on a deeper, ontological level that persistence of a phyletic line through geological time is the key measure of ecological success. For a species to have a higher probability of existence at any randomly chosen point in geological time has more meaning than for it to have a lower probability of existence, because the result is a greater potential to create new lines, influence other species: in short, to change the Earth. If this definition appears to emphasize group selection, the qualification is correct and justified. A great deal of macroevolution has occurred through the differentialextinction of species. * Based on the biennial Tansley Lecture of the British Ecological Society, given at Edinburgh on 18 December, 1985. 1: This content downloaded from 131.215.225.9 on Thu, 30 Jan 2014 22:59:41 PM All use subject to JSTOR Terms and Conditions 4~~~~~~~~~~~~~~~~~~N .....EDWAD.0 ILSO This content downloaded from 131.215.225.9 on Thu, 30 Jan 2014 22:59:41 PM All use subject to JSTOR Terms and Conditions 2 Tansley lecture to the B.E.S. The half-life of species is less than 10 million years in most taxonomic groups, and almost all species that ever lived have become extinct (Raup 1986). The effects on biotic composition and evolution made by the small fraction of surviving lines have been very great. If evolution is conceivably predictable even to a limited degree, it is likely to be made so in reality by picking out the successful living groups and characterizing their biological traits. Persistence of phyletic lines may in any case seem at first a spurious measure of 'success,' since all species existing today have a direct ancestry that goes all the way back to the origin of life. But what is meant is not persistence of the line relative to all life but rather persistence relative to other phyletic lines or 'clades' (Raup & Valentine 1983) that originated at about the same geological time and occupied the same major habitat. A sharply focused example is the following: if an adaptive radiation from one ancestral species in the Oligocene Epoch produced ten species, and only one survived as an evolving clade to the present time (perhaps speciating secondarily along the way), the one was more successful than the remaining nine. On the basis of the criterion of phyletic longevity the ants are relatively very successful. They have survived as a taxonomic family, the Formicidae, since the lowermost part of the upper Cretaceous, or about 100 million years B.P. All of the Cretaceous fossils belonging to the superfamily Formicoidea, in other words ants and their immediate ancestors, can be referred to the single formicid genus Sphecomyrma.The Sphecomyrmi- nae originate from localities across a wide portion of old Laurasia, from present-day Kazakhstan, north-central Siberia, and the Magadan region of easternmost Siberia to Alberta, Canada, and New Jersey, U.S.A. (Wilson 1985a, 1987a). Eomyrmex gucheng- ziensis, a species which I interpret to be intermediate between Sphecomyrma and the contemporary primitive subfamily Ponerinae, has been recorded from the early Eocene Fushan deposits of Manchuria (Hong et al. 1974). By mid-Eocene times, at least three modern subfamilies, the Myrmicinae, Dolichoderinae and Formicinae, had appeared, as represented by recently discovered fossils in the Arkansas amber (Wilson 1985a). By comparison with other animal groups, the Formicidae are older than nineteen of the twenty living mammalian orders (that is, all but the Marsupalia). Of the twenty mammalian families that apparently originated during the Cretaceous Period, only one, the Didelphidae or opossums, survived to the present time and hence are as old as the ants (Clemens et al. 1979). The Formicidae are also older than all living families of birds and all but three of the twenty-eight living orders (Phoenicopteriformes, Gruiformes, Charadrii- formes). Three of the bird orders originating in the Cretaceous, also those just listed, survive today, while the remaining two (Hesperornithiformes, Ichthyornithiformes) were confined to that geological period. These comparisons are impressive but of course wholly dependent on the similarity of orders and families as these categories are subjectively judged by taxonomists working independently on the insects and vertebrates respectively. At closer range, the ants are not exceptional among the families of the Hymenoptera. As shown in Table 1, no fewer thari twenty-five of the thirty-six families known from Cretaceous fossils, including the Formicidae, are still represented by living species. One remarkable group, the primitive sawflies of the family Xyelidae, have survived since the Triassic Period. Turning to the next lower taxonomic level, only one of the five ant genera (Iridomyrmex) thus far recorded from the Cretaceous and Eocene deposits is extant. However, no fewer than twenty-four genera, or 56% of the forty-three total representedin the early Oligocene Baltic amber ant fossils still survive, including such currently This content downloaded from 131.215.225.9 on Thu, 30 Jan 2014 22:59:41 PM All use subject to JSTOR Terms and Conditions E. 0. WILSON 3 TABLE1. Hymenopteranfamilies in the geologicalrecord, by periods(based on Carpenter1986) Triassic Jurassic Cretaceous Tertiary Extinct Recent Extinct Recent Extinct Recent Extinct Recent No. families 0 1 14 8 11 25 4 52 0/) Families 0 100 64 36 31 69 7 93 abundant and widespread taxa as Ponera, Tetraponera,Aphaenogaster, Monomorium, Iridomyrmex, Formica, Lasius, and Camponotus (Wheeler 1914). At least one species, Lasius schiefferdeckeri,is so close to living species of the L. niger group that it can be distinguished only by minor overlapping traits in antennal and mandibular form (Wilson 1955). This modern aspect is even more evident in the Dominican amber, which is apparently early Miocene in age. Here no fewer than thirty-four genera, or 92% of the total thirty-seven, still survive. Furthermore, the great majority of species thus far analysed have been placed in modern species groups, and in a few instances are difficult to separate at the species level (Wilson 1985b). Modern taxonomic studies of most other hymenopteran families in the Oligocene and Miocene deposits are still too incomplete to allow quantitative comparisons with the ants at the generic and specific levels. However, enough data are available on the Bethylidae and Braconidae of the Baltic amber to indicate percentages of generic survival comparable to that in the ants (see review by Larsson 1978). In summary, the ants are notable as a whole for their persistence as a clearly defined taxonomic family and hence of a clade that presumably originated as a single ancestral species during the Cretaceous Period. Genera and species groups, thought to represent radiations from post-Sphecomyrma lines, are also relatively ancient. The ants substan- tially exceed warm-blooded vertebrates in longevity at all taxonomic levels, but not, so far as the limited fossil data suggest, the families and genera of solitary Hymenoptera. Sheer longevity depends upon at least four general qualities at the population level, which will now be considered in turn. (1) Number of species generated through time. An ancestral line that penetrates many adaptive zones is more successful than one that survives as a single species, because through unintended effect it has 'balanced its investments' and ceteris paribus will probably persist longer into the future. The described world ant fauna consists of approximately 300 genera and 8800 species. The number of still unrecognized genera is evidently small. Judging from the rate of discovery during the past 50 years and the alacrity with which uncontestable novelties at the generic level are publicized, I would venture to guess that fewer than 100 still remain unrecognized.