Coevolutionary Race Research Articles

The Red King effect: when the slowest runner wins the coevolutionary race.

Mutualisms provide benefits to those who participate in them. As a mutualism evolves, how will these benefits come to be allocated among the participants? We approach this question by using evolutionary game theory and explore the ways in which the coevolutionary process determines the allocation of benefits in mutualistic interactions. Motivated by the Red Queen theory, which states that coevolutionary processes favor rapid rates of evolution, we pay particular attention to the role of evolutionary rates in the establishment of mutualism and the partitioning of benefits among mutualist partners. We find that, contrary to the Red Queen, in mutualism evolution the slowly evolving species is likely to gain a disproportionate share of the benefits. Moreover, population structure serves to magnify the advantage to the slower species.

The agricultural pathology of ant fungus gardens.

Gardens of fungus-growing ants (Formicidae: Attini) traditionally have been thought to be free of microbial parasites, with the fungal mutualist maintained in nearly pure "monocultures." We conducted extensive isolations of "alien" (nonmutualistic) fungi from ant gardens of a phylogenetically representative collection of attine ants. Contrary to the long-standing assumption that gardens are maintained free of microbial pathogens and parasites, they are in fact host to specialized parasites that are only known from attine gardens and that are found in most attine nests. These specialized garden parasites, belonging to the microfungus genus Escovopsis (Ascomycota: anamorphic Hypocreales), are horizontally transmitted between colonies. Consistent with theory of virulence evolution under this mode of pathogen transmission, Escovopsis is highly virulent and has the potential for rapid devastation of ant gardens, leading to colony mortality. The specialized parasite Escovopsis is more prevalent in gardens of the more derived ant lineages than in gardens of the more "primitive" (basal) ant lineages. Because fungal cultivars of derived attine lineages are asexual clones of apparently ancient origin whereas cultivars of primitive ant lineages were domesticated relatively recently from free-living sexual stocks, the increased virulence of pathogens associated with ancient asexual cultivars suggests an evolutionary cost to cultivar clonality, perhaps resulting from slower evolutionary rates of cultivars in the coevolutionary race with their pathogens.

Deep flowers for long tongues

Darwin[ 1 Darwin, C. (1862) On the Various Contrivances by which British and Foreign Orchids are Fertilized by Insects, John Murray Google Scholar ]explained deep-spurred flowers as adaptations to long-tongued pollinators. This spur elongation model was experimentally tested in some European orchids with rather short spurs[ 2 Nilsson L.A. Nature. 1988; 334: 147-149 Crossref Scopus (405) Google Scholar ]. The reciprocal effect in the coevolutionary race model[ 1 Darwin, C. (1862) On the Various Contrivances by which British and Foreign Orchids are Fertilized by Insects, John Murray Google Scholar ], postulating that the long tongues evolved as adaptation to exploit long-tubed flowers—favoured in Nilsson's news & comment article[ 3 Nilsson L.A. Trends Ecol. Evol. 1998; 13: 259-260 Abstract Full Text Full Text PDF PubMed Scopus (75) Google Scholar ]about my paper[ 4 Wasserthal L.T. Bot. Acta. 1997; 110: 1-17 Crossref Scopus (110) Google Scholar ]—has never been confirmed. The pollinator shift model[ 4 Wasserthal L.T. Bot. Acta. 1997; 110: 1-17 Crossref Scopus (110) Google Scholar ]is a modification of the spur elongation model, entailing the `driving force' of a nectar-exploiting competitor with a longer tongue than the `legitimate' pollinator(s). It was established after the following facts and arguments favouring the hypothesis that long tongues evolved for predator avoidance[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar , 6 Wasserthal L.T. Zoology. 1998; 101: 34 Google Scholar , 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar ]: •Individuals of European long-tongued hawkmoths (Agrius convolvuli) exhibited a swing-hovering behaviour and were incapable of inserting their tongues into long-tubed tobacco flowers[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]. •Swing-hovering has been discovered in almost all long-tongued Malagasy hawkmoths and recently in several related Central/South American species[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar , 6 Wasserthal L.T. Zoology. 1998; 101: 34 Google Scholar ]. •In primarily nonswinging individuals, swing-hovering could be induced by simulated predator stimuli[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]and ctenid spiders in Costa Rica. •Heteropodid spiders in Madagascar systematically pursue and jump at shivering or hovering moths[ 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar ]. •Long-tongued hawkmoths are generalist feeders; they skilfully exploit small and shallow flowers (e.g. of Verbenaceae[ 5 Wasserthal, L.T. (1993) in Animal–Plant Interactions in Tropical Environments (Barthlott, W. et al., eds), pp. 77–87, Zoologisches Forschungsinstitut und Museum Alexander Koenig, Bonn Google Scholar ]). •The Old World Xanthopan and the New World Cocytius are regarded as close relatives, with their very long tongue being a basic trait of ancestral Sphingicae and Acherontiicae[ 8 Rothschild L.W. Jordan K. Novit. Zool. 1903; 9: 1-972 Google Scholar ]. •Their hairy caterpillars feed on primitive angiosperms (Annonaceae)[ 7 Wasserthal, L.T. (1996) German Research Rept. DFG 1/96, 22–25 Google Scholar , 9 Moss A.M. Novit. Zool. 1920; 27: 334-415 Google Scholar ]. •The sphingophilous long-tubed flowers, especially the orchids, are of more recent origin, and the ancestors of their modern pollinators visited less-specialized flowers of older plant families[ 10 van der Pijl, L. and Dodson, C.H. (1966) Orchid Flowers, their Pollination and Evolution, University of Miami Press Google Scholar ].

The Pollinators of the Malagasy Star OrchidsAngraecum sesquipedale, A. sororiumandA. compactumand the Evolution of Extremely Long Spurs by Pollinator Shift

Abstract:The pollination process of the extremely long‐spurred orchidsAngraecum sesquipedaleandA. sororiumis described and documented here for the first time. The pollinaria and viscidia load was examined in moths captured in central and south Madagascar. Visits to orchids by hawkmoths were rarely observed in the field and were therefore systematically recorded in large flight tents using a night‐vision video technique and flashlight photography.Angraecum sesquipedalein Fort Dauphin is pollinated byXanthopan morgani praedictaandA. sororiumon Mt. Angavokely byCoelonia solani. By combining a deep nectar spur of extraordinary length with a protruding labellum functioning as a landing platform, these orchids overcome the moth's stereotypic swing‐hovering flight thus enabling full insertion of the long tongue.Angraecum compactumin Forêt d'Ambohitantely is pollinated by both the shorter and longer‐tongued forms ofPanogena lingenswhich never swing‐hover but is also exploited byX. morganiandC. solaniwith wastage of pollinaria. The duration of tongue insertion, nectar exploitation and tongue withdrawal were analyzed: legitimate and illegitimate visitors differ in their time budget and approach to the flower. Nectar volume, nectar level and sugar concentration ofA. sesquipedaleandA. sororiumwere compared with the nectar requirements of the pollinating hawkmoths. The evolution of very long spurs in these orchids is likely to have involved a series of pollinator shifts. The orchids adapted to different hawkmoth species with increasingly long tongues which primarily evolved to avoid predator attacks during visits to less specialized flowers. This “pollinator shift” model modifies the classical “coevolutionary race” model. The relevance of the taxonAngraecum bosseriSenghas is questioned.

Pathogen prevalence and human mate preferences

Members of host species in pathogen-host coevolutionary races may be selected to choose mates who possess features of physical appearance associated with pathogen resistance. Human data from 29 cultures indicate that people in geographical areas carrying relatively greater prevalences of pathogens value a mate's physical attractiveness more than people in areas with relatively little pathogen incidence. The relationship between pathogen prevalence and the value people place on physical attractiveness remained strong even after potential confounds such as distance from the equator, geographical region, and average income were statistically controlled for. Discussion focuses on potential limitations of the data, alternative explanations for the findings, and the nature of adaptions to the problems posed by pathogen prevalence.

Natural food requirements of the large milkweed bug,Oncopeltus fasciatus (Hemiptera: Lygaeidae), and their relation to gregariousness and host plant morphology.

The life ofOncopeltus fasciatus centers on the seeds of milkweeds (Asclepiadaceae,Asclepias syriaca in this study). Adults reproduce prolifically on these seeds, but they engage in only half as much copulation and lay only a few eggs when fed milkweed buds and flowers instead. They can not maintain body weight on a diet of just vegetative plants. Vegetative shoots support only slow growth and produce adults only in certain circumstances.Seeds are often inaccessible to nymphs in the three youngest instars, since their mouthparts are too short to penetrate the thick walls ofA. syriaca pods. Nymphs feeding from the outside of closed pods develop more slowly than those feeding on exposed seeds. Since mortality occurs at a constant rate, slow growth results in fewer surviving. Even adults, which can feed through almost any pod wall, prefer to feed where it is thinnest. Thus the pod wall effectively protects many seeds from this herbivore.Nymphs in larger groups (20 individuals) suffer much lower mortality than those in small groups (5 individuals), when they are feeding from the outside of closed pods. However, group size does not affect survival when nymphs are fed seed. Gregariousness apparently partly compensates for the less nutritious diet attainable from the outside of pods and thus is related to this bug's extreme specialization of diet.Other characteristics coordinated with the seed requirement include the timing of migration and egg laying, the female's choice of oviposition site, and the nymphs' balanced tendencies to be sedentary and to disperse. Among the milkweeds, such traits as thick pod walls, wide spacing, and rapid seed dispersal could have been selected for by a seed predator such asO. fasciatus.As a specialist and a probable agent of such selection,O. fasciatus is committed to keeping up with changes in its host plant. This requires maintaining some flexibility in its behavior or gene pool. K. Evans (personal communication) finds thatO. fasciatus in California onA. fascicularis lays eggs so early that the first nymphs hatch as the first flowers are opening. In that more equitable climate and on that host, adult reproduction is apparently not as dependent on pods being present in the colonized patch, and the nymphs must rely on non-seed food more often than they do in the association withA. syriaca in the East and Midwest. This very specialized species apparently retains enough adaptability to exploit milkweeds of various forms and phenologies living in a wide range of climates. This adaptability could promise its continued success in the coevolutionary race with its host plants.

Coevolutionary Race Continues: Butterfly Larval Adaptation to Plant Trichomes

Plant trichomes can act as efjective defenses against herbivores, but at least one species of ithomiid butterfly, Mechanitis isthmia, has evolved a unique adaptation for avoiding the trichomes on its spiny Solanum hosts. The larvae are gregarious all together they spin a fine silk scaffolding over the tops of the spines on which they can crawl and feed in safety.