BioScience 34(5): 326 (May1984)
Counterfeit Hybridization and Speciation
J. M. J. de Wet, C. A. Newell, and D. E. Brink

A condensation of “Counterfeit hybrids between Trisacum and Zea (Gramineae),” published recently in American Journal of Botany (Vol. 71, No. 2). The authors are members of the Crop Evolution Laboratory, Department of Agronomy, University of Illinois, 1102 South Goodwin, Urbana, IL 61801.

Species of Tripsacum (2n = 36, 72) cross with Zea mays L. (2n 20) when parents are not reproductively isolated by gametophytic or other barriers. When diploid Tripsacum (2n = 36) is used as the female parent, hybrids combine the cytologically reduced (18 chromosomes) or nonreduced (36 chromosomes) genome of Tripsacum and the cytologically reduced (10 chromosomes) or, more rarely, the nonreduced (20 chromosomes) genome of Zea.

Maternal offspring with 2n = 36 Tripsacum chromosomes resulting from parthenogenetic development of cytologically nonreduced female gametophytes are also produced. Some individuals with 2n = 36 Tripsacum chromosomes. however, are hybrid rather than maternal in phenotype. These counterfeit hybrids incorporated Zea genetic material into their Tripsacum genomes without true fertilization between the Tripsacum egg and Zea sperm.

Mutations induced by the presence of the Zea sperm in a Tripsacum embryosac are not random. Specific and repeatable phenotypic changes characterize counterfeit hybrids. Furthermore, similar maizoid traits appear in counterfeit hybrids between different species of Tripsacum and the same maize inbred. This suggests nonrandom transfer of Zea genes, or nonrandom incorporation of selected Zea DNA fragments into specific positions of the Tripsacum genome. These are not necessarily transposable elements. Several behave as stable genes in Zea and derivatives of counterfeit hybrids. Jumping seems to be in the nature of many normally stable genes.

Mechanisms of gene transfer between nonfunctional sperm and parthenogenetically developing eggs are unknown. Transfer of DNA probably takes place during early mitotic division of the egg. Exogenous DNA fragments introduced into the embryosac of angiosperms can become incorporated into the egg genome during fertilization or asexual development into an embryo. It is also possible, but less likely that actual fertilization takes place during counterfeit hybridization. and that the Zea chromosomes are eliminated during embryo development.

The evolutionary potential of counterfeit hybridization in nature is tremendous. Functional, cytologically reduced as well as nonreduced female gametes are commonly produced in diploid as well as polyploid plants. All that is further required is for an alien male gametophyte to compete successfully with a nonalien male gametophyte in reaching the ovary and for the foreign gametophyte to deposit its sperm into the embryosac at time of normal fertilization or parthenogenelic development of the egg. Offspring of Tripsacum-Zea counterfeit hybrids phenotypically resemble derivatives of experimentally induced introgression between Tripsacum and maize. Counterfeit hybridization probably accounts for much of the variation that characterizes T. dactyloides (L.) L., a species extending across the range of the genus from 42° N to 24° S latitude in the New World.

Counterfeit hybridization may also explain speciation. It is generally accepted that microevolution is an integral part of population survival. Mutation, immigration of gametes, seeds, and individuals from related populations, in conjunction with sexual reproduction, generate the genetic variations that allow populations to remain adapted to their ever-changing habitats. Adaptive radiation can initiate speciation. Speciation is achieved when subpopulations are no longer capable of free gene exchange. The origin of postfertilization reproductive isolation is difficult to explain. Counterfeit hybridization provides an ideal isolating mechanism. Counterfeit hybrids between Tripsacum and Zea differ from their Tripsacum parent in phenotype as well as cytological behavior. They produce sterile offspring when crossed with their maternal Tripsacum parent. Karyotype is not obviously altered, but chromosome pairing is incomplete. Tripsacum cundinamarce de Wet and Timothy (2n =36) probably originated as a counterfeit hybrid between T. dactyloides var, meridonale de Wet and Timothy and Zea mays as the pollen parent.