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Cytogenetic Aspects of Evolution of the Family Heteroderidae 1

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Cytogenetic Aspects of Evolution of the Family Heteroderidae 1 Cytogenetic Aspects of Evolution of the Family Heteroderidae 1 A. C. TRIANTAPHYLLOU 2 Cytotaxonomy implies the utilization of phylogenetic relationships of the members of cytological information in taxonomy. Such a group and have indicated the direction of information is mostly limited to the descrip- their evolution. The greatest phylogenetic tion of the karyotype, i.e., chromosome num- interpretation value of the karyotype is often ber, morphology, size, sex chromosomes, at the genus, and usually at or below the presence or absence of supernumerary or species level; this is because the causal rela- other types of chromosomes, and the study tionships of the observed karyotypic varia- of the behavior of the chromosomes during tions are easier to interpret at the genus or the mitotic and the meiotic cycle. With the species level due to a shorter evolutionary adoption of the biological species concept in time scale compared to that of higher taxa. animal taxonomy, however, it became neces- In keeping with the overall objectives of sary for species delineation to know the this symposium, I should probably discuss mode of reproduction of a particular orga- in general terms the role cytogenetic in- nism and its capabilities for effective inter- formation can play in solving problems in breeding with related organisms. To meet nematode taxonomy. A general discussion, the new requirements, cytotaxonomy ex- however, involving all nematodes would be tended its activities to include the study of difficult to comprehend, and would provide the mode of reproduction through karyologi- no solutions to specific taxonomic problems. cal analysis of gametogenesis, and the study For this reason I will limit this discussion of the behavior of the chromosomes in hy- to the family Heteroderidae, an important brids between related organisms. These new family of plant-parasitic nematodes, in which approaches are both cytological and genetic a good deal of cytogenetic work has been in nature. Therefore, in a broader definition, conducted recently. General conclusions will cytotaxonomy utilizes "cytogenetic" informa- undoubtedly be applicable to other families tion for elucidation of taxonomic problems. of nematodes with similar cytogenetic char- Analysis of the karyotype has been valu- acteristics. able in the study of the relationships within The central theme of this discussion is that evolution in the family Heteroderidae has several animal groups such as primates, in- been influenced by extensive modifications sects, rodents, etc. Karyotype comparisons of the basic karyotype, including the estab- have often permitted interpretations of the lishment of polyploidy and aneuploidy, in Received for publication 23 September 1969. association with the establishment of various 1 Paper number 2983 of the Journal Series of the North types of parthenogenetic reproduction. By Carolina State University Agricultural Experiment Station, studying the karyotypic relationships of the Raleigh, North Carolina. Supported by National Science Foundation Grant GB-7214. present day forms of these organisms, and 2 Department of Genetics, North Carolina State University at Raleigh, North Carolina 27607. considering other available cytogenetic in- 26 SYMPOSIUM: HETERODERIDAE; CYTOGENETIC EVOLUTION ° Triantaphyllou 27 formation, we may be able to make some Miller & Gray, H. mexicana Campos, and inferences as to the actual pathway of evolu- Osborne's cyst nematode. The karyotype tion of the family, and suggest a sound of all these species is quite similar. There taxonomic treatment. Of course, evaluation are some differences in chromosome mor- of the cytogenetic information alone, to the phology, chromosome size, and chromosomal exclusion of other available information, behavior during gametogenesis from species would share the same shortcomings of other to species, but, in the absence of a detailed taxonomic systems relying entirely on in- karyotypic analysis and comparison, such formation of one kind. A better system of differences are of limited value in character- classification may result, if all information izing the species or suggesting relationships available with regard to cytogenetics, mor- among them. phology, physiology, biochemistry, ecology, Another three species of Heterodera that behavior and distribution of these organisms have been studied cytologically, i.e., H. tri- is considered and evaluated at the same time. folii (Goffart), H. galeopsidis (Goffart), In the present discussion emphasis will be and H. lespedezae Golden & Cobb, as well placed on the following cytogenetic char- as an undescribed species from Rumex cris- acters: karyotype, chromosomal behavior pus L., are morphologically closely related during gametogenesis, and mode of repro- to H. schachtii and H. glycines and constitute duction. Certain morphological and phys- a series of chromosomal forms, with somatic iological characters will be considered in numbers ranging from 24 to 34, and re- some cases. produce by mitotic parthenogenesis (4). According to the latest taxonomic treat- There is tittle doubt that these "species" have ment, the family Heteroderidae comprises been derived from H. schachtii or H. glycines five genera, Heterodera A. Schmidt, Meloi- through various chromosomal changes lead- dogyne Goeldi, Meloidodera Chitwood, Han- ing to polyploidy and aneuploidy in associa- non & Esser, Cryphodera Colbran, and tion with the establishment of parthenogenetic Meloidoderita Poghossian. A sixth genus, reproduction (Table 1). It is very likely Hypsoperine Sledge & Golden, was synony- that all of them have evolved along the same mized with Meloidogyne in 1968 (15), phyletic line, or a number of parallel phyletic but a new species described early in 1969 lines derived from the same basic species was placed in Hypsoperine as H. ottersoni or group of related species, at different Thorne (8). No cytogenetic work has been occasions and probably at different time done with the monotypic Cryphodera and periods. They constitute a parthenogenetic Meloidoderita, and therefore, these genera species complex completely separated re- will not be included in the discussion. productively and, therefore, genetically from Among the species of Heterodera studied the amphimictic species from which they thus far cytologically, 13 are diploid amphi- have been derived. mictic with a haploid number of 9 chromo- From a taxonomic viewpoint, it is an open somes. These include H. schachtii A. question whether members of such a par- Schmidt, H. glycines Ichinohe, H. oryzae thenogenetic species complex should be Luc & Brizuela, H. avenae Wollenweber, H. treated as separate species (as has been done goettingiana Liebscher, H. cruciferae Frank- in the past in nematode taxonomy) without tin, H. carotae Jones, H. weissi Steiner, H. reference to their phylogenetic relationships, rostochiensis Wollenweber, H. tabacum should be regarded as subspecies (14) or as Lownsbery & Lownsbery, H. virginiae properly designated, but unnamed, infra- 28 Journal o[ Nematology, Vol. 2, No. 1, January 1970 specific categories of the same parthenoge- H. betulae indicates that the karyotype of netic species. Nematode taxonomists need to this species has not yet stabilized. Further- find a practical solution to this problem, and more, the occasional appearance of males, at the same time to decide which of the and the meiotic type of maturation of the theoretically numerous morphological and oocytes suggest that reproduction by cross- physiological variants within a parthenoge- fertilization may occur occasionally in this netic group should be recognized as separate species. Consequently, the instability of the taxonomic entities. karyotype, and the facultative type of par- A similar case of parthenogenetic evolu- thenogenesis, would tend to indicate that H. tion in the genus Heterodera involves H. betulae has been derived recently and is still oryzae and H. sacchari Luc & Merny of the in a state of active evolution. This is in H. schachtii species group. These two species contrast to the evolutionary status of the are very closely related morphologically and H. trifolii species complex, in which the have the same geographical distribution. H. complete absence of males, and the obliga- oryzae is a diploid amphimictic species with tory type of mitotic parthenogenesis indicate n = 9 chromosomes, whereas, H. sacchari an advanced state of evolution (although has 2n = 27 and reproduces by mitotic par- degenerative evolution), with no spectacular thenogenesis (6). It is very likely that H. changes being expected in the future. sacchari has evolved from H. oryzae, or These, briefly, are the three separate lines another amphimictic relative as a triploid of parthenogenetic evolution observed thus parthenogenetic form (Table 1 ). H. leuce- far in the genus Heterodera. ilyma Di Edwardo & Perry, is closely related In the genus Meloidodera, the only species morphologically to H. sacchari, has no males studied cytogenetically, M. floridensis Chit- and undoubtedly reproduces by partheno- wood, Hannon & Esser, reproduces by genesis. Although no cytological work has mitotic parthenogenesis and has a somatic been done with H. leuceilyma, it very likely chromosome number of 26 and 27 (A. C. has evolved along the same parthenogenetic Triantaphyllou, unpublished data). Its chro- line with H. sacchari and, consequently, be- mosomes resemble those of mitotic partheno- longs to the same parthenogenetic species genetic species of Heterodera, like H. trifolii, complex.
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