GENETIC CONSTRAINTS ON MACROEVOLUTION - THE EVOLUTION OF HOST AFFILIATION IN THE LEAF BEETLE GENUS OPHRAELLA

We hypothesize that the evolution of an ecologically important charact er, the host associations of specialized phytophagous insects, has bee n influenced by limitations on genetic variation. Using as a historica l framework a phylogenetic reconstruction of the history of host assoc iations in the beetle genus Ophraella (Chrysomelidae), we have employe d quantitative-genetic methods to screen four species for genetic vari ation in larval survival, oviposition (in one species only), and feedi ng responses to their congeners' host plants, in the Asteraceae. We he re report results of studies of one species and evaluate the results f rom all four. Analysis of half-sib/full-sib families and of progenies of wild females of O. notulata, a specialist on Iva (Ambrosiinae), pro vided evidence of genetic variation in larval consumption of five of s ix test plants and in adult consumption of four of six. Larval mortali ty was complete on five plants; only on Ambrosia, a close relative of the natural host, was there appreciable, and genetically variable, sur vival. Oviposition on Ambrosia showed marginally significant evidence of genetic variation; a more distantly related plant elicited no ovipo sition at all. In compiling results from four Ophraella species, repor ted in this and two other papers, we found no evidence of genetic vari ation in 18 of 39 tests of feeding responses and 14 of 16 tests of lar val survival on congeners' hosts. This result is consistent with the h ypothesis that absence or paucity of genetic variation may constrain o r at least bias the evolution of host associations. The lower incidenc e of genetic variation in survival than in feeding behavior may imply, according to recent models, that avoidance is a more common evolution ary response to novel plants than adaptation. The usually great dispar ity between mean performance on congeners' hosts and the species' natu ral hosts, and an almost complete lack of evidence for negative geneti c correlations, argue against the likelihood that speciation has occur red by sympatric host shift. The presence versus apparent absence of g enetic variation in consumption was correlated with the propinquity of relationship between the beetle species tested and the species that n ormally feeds on the test plant, suggesting that the history of host s hifts in Ophraella has been guided in part by restrictions on genetic variation. It was also correlated with the propinquity of relationship between a test plant and the beetle's natural host. The contributions of plant relationships and insect relationships, themselves correlate d in part, to the pattern of genetic variation, are not readily distin guishable, but together accord with phylogenetic evidence that these a nd other phytophagous insects adapt most readily to related plants. In this instance, therefore, the macroevolution of an ecologically impor tant character appears to have been influenced by genetic constraints. We hypothesize that absence of the structural prerequisites for genet ic variation in complex characters may affect genetic variation and th e trajectory of evolution.