letters to nature

20. Leakey, R. E. & Leakey, M. G. A new hominoid from Kenya. Nature 342, 143–146 (1986). 21. Leakey, M. G., Leakey, R. E., Richtsmeier, J. T., Simons, E. L. & Walker, A. C. Similarities in Aegyptopithecus and Afropithecus facial morphology. Folia Primatol. 56, 65–85 (1991). 22. Delson, E. & Andrews, P.in Phylogeny of the : A Multidisciplinary Approach (eds Luckett, W. P. & Szalay, F. S.) 405–446 (Plenum, New York, 1975). 23. Strasser, E. & Delson, E. Cladistic analysis of cercopithecid relationships. J. Hum. Evol. 16, 81–99 (1987).

Acknowledgements. Excavations at Maboko were conducted with permission of the Office of the President, Republic of Kenya and in collaboration with the National Museums of Kenya. We thank the field crew (especially B. Onyango, V. Oluoch and S. Gitau) and M. G. Leakey for assistance, and E. Delson, M. Kohler, S. Moya-Sola and D. Pilbeam for comments and advice. This work was supported by NSF, L. S. B. Leakey Foundation, National Geographic Society, Wenner Gren Foundation for Anthropological Research, Fulbright, and Boise Fund.

Correspondence and requests for materials should be addressed to B.R.B. (e-mail: bbenefi[email protected]).

Apparent competition structures ecological assemblages

M. B. Bonsall & M. P. Hassell Department of Biology and the NERC Centre for Population Biology, Imperial College at Silwood Park, Ascot, Berkshire SL5 7PY, UK ...... Competition is a major force in structuring ecological com- munities1. It acts directly2 or indirectly, in which case it may be mediated by shared natural enemies and is known as ‘apparent 3–6 Figure 3 Bivariate plot of log10-transformed mean brain and body weight data for competition’ . The effects of apparent competition on species extant hominoids (H), cercopithecoids (C), platyrrhines (P), tarsiers (T), lemuroids coexistence are well known theoretically7,8 but have not previously and lorisoids (L)14, Victoriapithecus and Aegyptopithecus. Superimposed best fit been demonstrated empirically in controlled multigenerational lines for extant anthropoids (higher) and strepsirhines (lower) are based on least- experiments. Here we report on the population dynamic conse- squares linear regression equations. quences of apparent competition in a laboratory insect system with two host species and a common parasitoid attacking them. We find that whereas the two separate, single host–single para- catarrhine features, rather than derived indicators of affinity with sitoid interactions are persistent, the three-species system with the great and human clade. In this way, the Victoriapithecus skull the parasitoid attacking both hosts species (which are not allowed shows that the anatomy of cercopithecoids is as important as to compete directly) is unstable, and that one of the host species is that of hominoids for deciphering the evolutionary history of Old eliminated from the interaction owing to the effects of apparent World higher primates. Ⅺ competition. Received 21 November 1996; accepted 30 May 1997 Classical ecological theory predicts that simple interactions in 1. Pilbeam, D. R. New hominoid skull material from the Miocene of Pakistan. Nature 295, 232–234 which species share common natural enemies are unstable, leading 9 (1982). to one species being eliminated from the interaction . This effect 2. Brown, B. & Ward, S. in Orang-utan Biology (ed. Schwartz, J. H.) 247–260 (Oxford Univ. Press, New arises through competitive interactions mediated by the natural York, 1988). 7,8 3. Moya-Sola, S. & Kohler, M. Recent discoveries of Dryopithecus shed new light on evolution of great enemy in ‘apparent competition’ . As the two host species are not . Nature 365, 543–545 (1993). directly competing for resources, the loss of one of the species results 4. Moya-Sola, S. & Kohler, M. New partial cranium of Dryopithecus Lartet, 1863 (Hominoidea, Primates) from the upper Miocene of Can Llobateres, Barcelona, Spain. J. Hum. Evol. 29, 101–139 solely from the dynamic consequences of the natural enemy (1995). becoming more abundant as a consequence of having an alternative 5. Von Koenigswald, G. H. R. Miocene Cercopithecoidea and Oreopithecoidea from the Miocene of East host species. The species that persists in the interaction is the one . Foss. Vert. Afr. 1, 39–51 (1969). 6 6. Benefit, B. R. & McCrossin, M. L. Ancestral facial morphology of Old World higher primates. Proc. that can support the higher parasitoid density . Natl Acad. Sci. USA 88, 5267–5271 (1991). These indirect competitive interactions have received little atten- 7. Benefit, B. R. The permanent dentition and phylogenetic position of Victoriapithecus from , Kenya. J. Hum. Evol. 25, 83–172 (1993). tion from natural or laboratory systems, although they are likely to 8. Benefit, B. R. Phylogenetic, paleodemographic and taphonomic implications of Victoriapithecus be as important, if not more so, than direct competitive interac- deciduous teeth from Maboko, Kenya. Am. J. Phys. Antropol. 95, 277–331 (1994). tions. Empirical work so far has focused mainly on short-term, 9. Feibel, C. S. & Brown, F. H. Age of the -bearing deposits on Maboko Island, Kenya. J. Hum. Evol. 21, 221–225 (1991). behaviourally orientated studies in which natural enemy responses 10. Andrews, P., Meyer, G., Pilbeam, D. R., Van Couvering, J. A. & Van Couvering, J. A. H. The Miocene are recorded within a single field season of the interaction10–15.No fossil beds of Maboko Island, Kenya: Geology, age, taphonomy and paleontology. J. Hum. Evol. 10, 35–48 (1981). empirical studies have addressed directly the long-term effects of 11. Stromer, E. Mitteilungen uber die Wirbeltierreste aus dem Mittelpliocan des Natrontales (Agypten). apparent competition on the population dynamics of the interact- 1. Affen. Z. Deutsch. Geol. Gesell. Abh. 65, 349–361 (1913). ing organisms. We now report on the temporal consequences of 12. Harrison, T. New postcranial remains of Victoriapithecus from the middle Miocene of Kenya. J. Hum. Evol. 18, 3–54 (1989). such apparent competition (Figs 1, 2). A series of long-term 13. Radinsky, L. The fossil evidence of anthropoid brain evolution. Am.J.Phys.Anthropol.41, 15–28 (1974). laboratory experiments were used to explore the interaction 14. Martin, R. D. Primate Origins and Evolution (Princeton Univ. Press, Princeton, NJ, 1990). 15. Benefit, B. R. & McCrossin, M. L. The facial anatomy of Victoriapithecus and its relevance to the between the ichneumonid parasitic wasp Venturia canescens ancestral cranial morphology of Old World monkeys and apes. Am.J.Phys.Anthropol.92, 329–370 (1993). (Gravenhorst) and two of its moth hosts, Plodia interpunctella 16. Vogel, C. Morphologische studien am gesichtschadel Catarrhiner primaten. Biblio Primatol. 4, 1–226 (Hubner) and Ephestia kuehniella Zeller, over a period of several (1966). 17. Harrison, T. The phylogenetic relationships of the early catarrhine primates: A review of the current generations. The direct competitive effects between the host evidence. J. Hum. Evol. 16, 41–80 (1987). species were fully excluded by a vertical barrier of nylon mesh 18. Simons, E. L. The earliest apes. Sci. Am. 217, 28–35 (1967). 19. Simons, E. L. New faces of Aegyptopithecus from the Oligocene of Egypt. J. Hum. Evol. 16, 273–289 dividing each cage in half. The mesh size was large enough to (1987). allow free access for the searching parasitoids between the two

NATURE | VOL 388 | 24 JULY 1997 Nature © Macmillan Publishers Ltd 1997 371 letters to nature

Figure 1 Representative examples of the population dynamics of the single host-single parasitoid interac- tions: a, b, P.interpunctella (dotted line)–V. canescens (dashed line); c, d, E. kuehniella (unbroken line)–V. canescens (dashed line). Experiments were carried in cages (30 ϫ 30 ϫ 30 cm) under standard environmen- tal conditions (25 Ϯ 2 ЊC; 70 Ϯ 5% R.H. 16 : 8 h light– dark cycle). Linear time series analysis indicates an underlying tendency for oscillations dampening towards a stable equilibrium.

Figure 2 Representative examples of the population dynamics of the three species system of two hosts and a single parasitoid: P. interpunctella (dotted line)–E. kuehniella (unbroken line)–V. canescens (dashed line). In all these cases, E. kuehniella is eliminated from the interaction by the action of the shared natural enemy, V. canescens. Time series analysis now indicates damped oscillations for the interaction between P. interpunctella and V. canescens and diverging oscillations for E. kuehniella.

halves, but was too small to let the hosts pass through. The between the two apparently competing host species (P. interpunc- interactions with a single host and single parasitoid, and the more tella and E. kuehniella) is amensal: the effect of P. interpunctella on E. complex three-species interactions of two hosts and a single kuehniella is strong whereas the reciprocal effects of E. kuehniella on parasitoid, were each replicated eight times and monitored over P. interpunctella is negligible (Fig. 3). P. interpunctella is dominant 15 generations by weekly census counts of dead adults16. because it has a larger intrinsic rate of increase and shorter In all the two-species systems, the two populations persisted in development time16. relatively stable interactions (Fig. 1). Time-series statistics show that Such asymmetric relationships in the interaction strengths have the dynamics in these cases were largely driven by delayed density- been widely documented for direct competition2 and also recorded dependent processes (primarily due to the parasitoids) and predict in one case for an indirect interaction17. If shown to be normal for damped oscillations to a stable equilibrium. In contrast, the full indirect competitive interactions as well, amensal apparent compe- three-species interaction of P-interpunctella–E. kuehniella–V. canes- tition may prove to be a key process for structuring ecological cens never persisted (Fig. 2), and in all cases E. kuehniella was always assemblages. It could, for example, play a central part in the rapidly eliminated from the system by the action of the shared persistence of species assemblages made up of a single dominant natural enemy. Time-series statistics again show that the population species (free from the effects of direct and apparent competition) dynamics of the three species were governed by delayed density and many rarer species reduced in abundance by the effects of dependence. But now E. kuehniella is predicted to show divergent indirect amensal interactions. oscillations while P. interpunctella and V. canescens show damped We have demonstrated empirically the long-term population oscillations towards a stable equilibrium. The parasitoid V. canes- effects of two species sharing a natural enemy. The resulting cens thus directly restricts the number of host species that it attacks, extinction of one of the host species mimics direct competition, a phenomenon known as ‘dynamic monophagy’6. although direct competitive effects are absent. Such indirect effects The results reveal interesting properties of the interactions. A could be very important for the dynamics of species assemblages if repeated-measures analysis of variance shows that the interaction they are widespread under natural conditions. Host–parasitoid

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a b

0.3 Genetic interaction between 0.6 male mating strategy and

0.2 sex ratio in a marine isopod

0.4 density density Stephen M. Shuster* & Clay Sassaman†

Plodia * Department of Biological Sciences, Northern Arizona University, Flagstaff, x Ephestia 0.2 x 0.1 Arizona 86011-5640, USA x † Department of Biology, University of California, Riverside, California 92521, USA x ...... Individual males in many species exhibit discrete modes of 0.0 0.0 behaviour1–3, but the genetic mechanisms underlying these differ- + Ephestia – Ephestia + Plodia – Plodia ences are poorly understood. Here we investigate the genetics of the isopod crustacean Paracerceis sculpta, in which three different Figure 3 Box plots for a, E. kuehniella, and b, P.interpunctella in the presence (þ) types of males coexist, each distinguishable from the others by 4,5 or absence ( Ϫ ) of the other host species. The solid line within each box marks the their behavioural and morphological phenotypes . Within median; the cross marks the mean value. The length of the box is the interquartile families, alleles of the gene encoding the enzyme phosphogluco- range and the limit bars show the distance to 1.5 times the interquartile range mutase (Pgm gene) are associated with particular male pheno- giving a measure of dispersion in the data. The plots show the density of each types, although no significant association between these species over a nine-week period. A repeated-measures analysis of variance characters exists population-wide. This suggests that Pgm is (following a square-root transformation) reveals that the interaction mediated via closely linked to a single genetic locus which controls male the shared parasitoid, V. canescens, is amensal. The effects of apparent phenotype. We call this the alternative mating strategy (Ams) competition are extremely skewed, with one host suffering very little while the locus. We present evidence that two other factors—an autosomal other is driven to extinction. gene, transformer (Tfr), and an extrachromosomal factor—inter- act with primary sex determination loci and with alleles at Ams, causing certain individuals to change sex, thereby biasing family assemblages may be particularly prone to these indirect effects sex ratios. A model based on our genetic analysis suggests that: (compare with other natural enemy–victim systems) because para- first, polymorphism in male behaviour is controlled by the sitoids tend to have a pronounced numerical response and to limit mendelian segregation of three alleles at the Ams locus; second, host population sizes well below their carrying capacities18. General- that family sex ratio is influenced by alternative alleles at the Tfr ist predators, on the other hand, will often show weaker numerical locus whose expression is influenced by the extrachromosomal responses to particular prey species and therefore be less likely to factor; and third, that Tfr and Ams interact epistatically to cause species exclusion through apparent competition19. Ⅺ determine the sex of the individual and, if male, its behaviour and external morphology. Received 17 March; accepted 28 April 1997. Females are monomorphic in P. sculpta. Males, however, exhibit 1. Law, R. & Watkinson, A. R. in Ecological Concepts (ed. Cherrett, J. M.) (Blackwell Scientific, London, ␣ 1989). three distinct morphs that differ in reproductive behaviour: - 2. Lawton, J. H. & Hassell, M. P. Asymmetrical competition in insects. Nature 289, 793–795 (1981). males are largest and defend harems within sponges using elongated 3. Menge, B. A. Indirect effects in marine rocky intertidal interaction webs—patterns and processes. posterior appendages; ␤-males invade harems by mimicking female Ecol. Monogr. 65, 21–74 (1995). 4. Strauss, S. Y. Indirect effects in community ecology: their definition, study and importance. Trends behaviour and morphology; and ␥-males invade harems by being Ecol. Evol. 6, 206–210 (1991). small and secretive5,6. A genetic model has been proposed7 to explain 5. Wootton, J. T. The nature and consequences of indirect effects in ecological communities. Annu. Rev. Ecol. Sys. 25, 443–466 (1994). the persistence of the three male morphs at stable frequencies, in 6. Holt, R. D. & Lawton, J. H. Apparent competition and enemy-free space in insect host–parasitoid which three alleles at a single autosomal locus (Ams) show direc- communities. Am. Nat. 142, 623–645 (1993). tional dominance and mendelian inheritance. 7. Holt, R. D. Predation, apparent competition and the structure of prey communities. Theor. Pop. Biol. 7 12, 197–229 (1977). We tested this model for male morphology using controlled 8. Holt, R. D. Spatial heterogeneity, indirect interactions and the coexistence of prey species. Am. Nat. laboratory crosses. We first examined mendelian inheritance at the 124, 377–406 (1984). 8 9. Williamson, M. H. An elementary theory of interspecific competition. Nature 180, 422–425 (1957). Pgm locus in 25/31 F1 families in which one heterozygous and one 10. Mu¨ller, C. B. & Godfray, H. C. J. Apparent competition between two aphid species. J. Anim. Ecol. 66, homozygous parent were crossed. As three alleles were detectable at 57–64 (1997). , we summarized alleles possessed by heterozygous parents as 11. Karban, R., Houghen-Eitzmann, D. & English-Loeb, G. Predator-mediated apparent competition Pgm between two herbivores that feed on grapevines. Oecologia 97, 508–511 (1994). allele 1 or allele 2. The total numbers of progeny possessing these 12. Settle, W. H. & Wilson, L. T. Invasion by the variegated leafhopper and biotic interactions: parasitism, allele classes were 405 and 424, respectively, and individual crosses competition and apparent competition. Ecology 71, 1461–1470 (1990). : : : 13. Schmitt, R. J. Indirect interactions between prey: apparent competition, predator aggregation and were homogeneous (G-test (ref. 9), GH ¼ 31 01) (d f ¼ 24, habitat segregation. Ecology 68, 1887–1897 (1987). P Ͼ 0:10). We considered Pgm inheritance to be mendelian. 14. Hanley, K. A., Vollmer, D. M. & Case, T. J. The distribution and prevalence of helminths, coccidia and The genetic model7 suggested that field-collected ␤- and ␥-males blood parasites in two competing species of gecko: implications for apparent competition. Oecologia 102, 220–229 (1994). are heterozygous at the Ams locus, and thus should produce 50 : 50 15. Grosholz, E. D. Interactions of intraspecific, interspecific and apparent competition with host– ratios of ␣- and ␤-, or ␣- and ␥-male sons, respectively, when pathogen dynamics. Ecology 73, 507–514 (1992). ␤ 16. Bonsall, M. B. Temporal and Spatial Insect Population Dynamics Thesis, Univ. London (1997). crossed with field-collected females (see Methods). As most - and 17. Evans, E. W. & England, S. Indirect interactions in biological control of insects: pests and natural ␥-males were also heterozygous at the Pgm locus (11/13 and 7/10, enemies in alfalfa. Ecol. Appl. 6, 920–930 (1996). respectively), we examined the association between genotype 18. Beddington, J. R., Free, C. A. & Lawton, J. H. Characteristics of successful natural enemies in models of Pgm biological control of insect pests. Nature 273, 513–519 (1978). and male phenotype among F1 progeny. If these loci were unlinked, 19. Holt, R. D. in Multitrophic Interactions in Terrestrial Systems (eds Gange, A. C. & Brown, V. K.) we expected the progeny of males heterozygous at both loci to (Blackwell Scientific, London, 1996). segregate four combinations of the two male morphs and two Pgm Acknowledgements. We thank R. Holt for comments on an earlier version of the manuscript. This work genotypes in equal frequency. The more severe the deviation from was supported by an NERC studentship to M.B.B. and an NERC-funded research grant to M.P.H. this expectation, the closer the linkage, thus, parental and recombinant 9 Correspondence and requests for materials to be addressed to M.B.B. (e-mail: [email protected]). classes were each pooled, then compared using a G-test (d:f: ¼ 1) .

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