Niilo Virkki, Jorge A. Santiago-Blay, and Shawn M. Clark.
Chromosomes of some Puerto Rican Disonychina and Oedionychina Coleoptera: Chrysomelidae: Alticinae: Oedionychini): Evolutionary implications.
Psyche 98:373-390, 1991.

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CHROMOSOMES OF SOME PUERTO RICAN
DISONYCHINA AND OEDIONYCHINA
(COLEOPTERA: CHRYSOMELIDAE: ALTICINAE:
OEDIONYCHINI):
EVOLUTIONARY IMPLICATIONS
BY NIILO VIRKKI~ , JORGE A. s ANTIAGO-BLAY' AND SHAWN M. CLARK^
Bechynk and Springlova de Bechynk (1966) divided the tribe Oedionychini into the subtribes Disonychina and Oedionychina based, mainly, on thoracic and hind tarsal structures. This classifi- cation is supported also on cytological grounds (Virkki 1988b, 1989b). The Oedionychini, a lineage that shows some of the most interesting chromosomal relationships within the Coleoptera (Smith and Virkki 1978, Virkki 1985, 1988a, 1989a), is cytologi- cally characterized by asynaptic sex chromosomes in male meiosis, increased spermatocyte size, and, in correlation with it, fewer sper- matozoa per bundle (spzlb ) (Virkki l988a). The inferred polarity of the last character points to Oedionychina (spz/b=16) as rela- tively derived (Disonychina, spz/b=32). The Oedionychini is con- sidered the most derived tribe of the Alticinae (J. Bechynk 1968 pers. comm.). A correlation of characters on the internal reproduc- tive system of the Chrysomelidae has recently been discussed by Suzuki (1989).
Meiograms and chromosomal illustrations of four Puerto Rican Disonychina and three Oedionychina are presented. Phylogenetic implications of these finds are discussed. ' Department of Crop Protection, Agricultural Experiment Station, P. 0. Box 21360, Rio Piedras, PR 00928-1360
Department of Entomological Sciences, University of California, Berkeley, CA 94720-0001 USA
West Virginia Department of Agriculture, State Capitol, Charleston, WV 25305 USA
Manuscript received 8 March 1991.




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Species, host plants (author and family), sample size, and collecting data are as in Table 1. Nomenclature and protocols fol- low Virkki, et al. (1992).
Disonychina. This Neotropical subtribe (Bechyne and Springlovk de Bechynk 1966) comprises seven genera of which, only two, Disonycha Blake and Phenrica Bechyne, have been par- tially studied cytologically (Virkki 1989b). Autosomes (13-30 pairs) have been found to combine with a sex chromosome system consisting of one Xy bivalent and one or two additional, univalent, X chromosome(s) (Xy+nX, n=l or 2).
Disonycha spilotrachela Blake
This is perhaps the most polyphagous Puerto Rican Disonycha (Table 1). A dense and persisting population feeds on Turnera ulmifolia (Turneraceae) on the south coast of Laguna Tortuguero. This species has been reported for Cuba, Haiti, and Puerto Rico (Wolcott 1948; Blake 1933, 1955; Wilcox 1983). Meiogram (Fig. 1A) and MI (Fig. 2B): 13+Xiy+X2. The segre- gation results in 15(2X) and in 14(y) chromosomes at M I1 plates (Figs. 3E, F, respectively).
Karyogram (Virkki 1988 b): 2n=30(4X) on females, 2n=29(2X7y) on males. All chromosomes are metacentric. Nucleo- lar organizing regions (NOR'S) are located on a homologous pair of medium-sized autosomes.
Disonycha comma White
This species also lives on Hispaniola, and perhaps has invaded Puerto Rico recently. Possibly, D. comma is synonymous with D. peruana Jacoby that inhabits mainland areas of tropical America. The first Puerto Rican specimens were collected in 1988 and now it is becoming common in the south coast of Laguna Tortuguero where it thrives on Croton lobatus (Euphorbiaceae), a common weed. In captivity, it has accepted only Passiflora murucuja (Pas- sifloraceae) among the various Passiflora spp. offered (J. Escudero 1989 pers. comm., see also Jolivet 199 1).



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Table 1. Species, plant association, and collection data for specimens examined. +
'-0
w F
Taxon Plant Association # Examined Collection Data a
for each locality
Disonychina
Disonycha spilotrachela Blake
Disonycha comma White
Disonycha leptolineata Blatchley
Disonycha eximia Harold
Oedionychina
Omophoita cyanipennis F.
Omophoita albicollis F.
Alagoasa bicolor (L.)
Ipomoea imperati (Vahl) Griseb. 20
(Convolvulaceae)
Turnera ulmfolia L. (Turneraceae) >50
Passflora foetida L. (Passifloraceae) 10 Croton lobatus L. (Euphorbiaceae) 10
Unidentified low herbs 1
Amaranthus sp. (Amaranthaceae) 20
Clerodendrum aculeatum (L.) Schlecht
>50; >50
(Verbenaceae)
Phyla nodiflora (L.) Greene
>5 0
(Verbenaceae)
Heliotropium indicum L. >20
(Boraginaceae)
Stachytarpheta jamaicensis (L.) Vahl >lo; >10 (Verbenaceae)
Chlerodendrum aculeatum (L.) Schlecht >lo0 (Verbenaceae)
Aegiphila martinicensis Jacq. >50
(Verbenaceae)
Isabela, Playa de Jobos, 1 Feb. 86
Vega Baja, Laguna Tortuguero,
Jan. 87-June 88
Gufinica, Laguna de Gufinica, 8 Oct. 87
Vega Baja, Laguna Tortuguero,
Aug.-Oct. 89
s
Ponce, Playa de Ponce, 2 Mar. 87
%
Dorado, rd. 165, Nov.-Dec. 84
5
2
a
<--K
Salinas, Playa de Salinas, 1962-85;
Carolina, Vacia Talega, 1962-85
Salinas, Playa de Salinas, 1962-85
Salinas, Playa de Salinas, Ju1.-Dec. 69
Mona Is., airstrip, 8 Mar. 84; Vega Baja, Tortuguero airport, 5 July 87
Salinas, Playa de Salinas, 1962-85
Vega Alta, rd. 675, 1973-85




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376
A
B
c
D
Fig. 1
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yi?t~l!ig(~~* ,^ Wd@' &, lift ?
Meiograms of some Puerto Rican Disonychina. A. Disonycha spilotra- chela, 13+Xjy+X2. B. D. comma, 18+X,y+X2. C. D. leptdineata, 19+X,y+X2. D. D. exirnia, 1 9+Xiy+X2+X3.
Meiogram (Fig. 1B) and M I (Fig. 2C): 18+Xly+X,. All auto- somes are metacentric and most are capable of forming ring biva- lent~, a sign of more than one crossover on a chromosome. Karyogram (Figs. 4, 5): 2n=40(4X) on females, 2n=39(2X,y) on males. All autosomes and, at least, XI are inetacentric. Disonycha leptolineata Blatchley
Formerly unknown from Puerto Rico, this species became quite abundant in the Ponce region some years ago (J. Micheli 1990 pen. comm.) but it is seldom seen nowadays. This population growth pattern suggests a recent invasion, followed by a rapid increase, and an effective checking by natural enemies (van den



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19911 Virkki et al. 377
Fig. 2. First meiotic metaphase in three Disonycha spp. Phase contrast. On A and B, the lowermost arrows point the X[y; on C, the right hand arrow. A. D. lepfolia- emu, l9+X, y+X2. (1435x1 3. W. spiiotrachela, 13+X, y+X2, (1 16BX) C. D. comma, 18+X,y+Xp (120SX)
Bosch, et al. 1982). This species is known from the U.S.A. to Mexico and Guatemala,
Meiogram (Fig. 1C) and M I (Fig. 2A): 19+Xiy+X2. This is an amendment of the former preliminary count 18+Xiy+X, (Virkki 1988b). The "telephone-handle'' shape of many bivalents suggests that they are formed by metacentric autosomes. Segregation to 2 l(2X) and 20(y) is confirmed by M I1 (Fig, 3A and B).



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Fig. 3. Second meiotic metaphase in three Disonycha spp. Phase contrast. Identi- fication of the sex chromosomes is not attempted. A and B. D. leptolineata. (1264X and 1018X, respectively.) A shows 21 chromosomes (19 autosomes, two X chro- mosomes); B, 20 chromosomes (19 autosomes and one y chromosome). C and D. D. eximia. (1018X) C shows 20 chromosomes (19 autosomes and one y chromosome); D, 22 chromosomes (19 autosomes and three X chromosomes). E and F. D. spilo- trachela 1791X) E shows 15 chromosomes (13 autosomes and two X chromo- somes); F, 13 autosomes and one y chromosome.



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19911 Virkki et al. 379
Fig. 4. Karyogram of female D. comma. 2n=40(4X). Disonycha eximia Harold
Apart from D. chlorotica (Olivier) and D. weisei Csiki, both of which likely belong in other genera and neither of which has been recognized in recent years, this is the only non-vittate Disonycha (Blake 1955) known from Puerto Rico. This species is distributed from Costa Rica to Panama. Wolcott (1948) suspected that this species may have arrived from Hispaniola in Puerto Rico early in the century. Undoubtedly, this species is now well established in Puerto Rico.
Meiogram (Fig. ID) and M I (Virkki 1988b): 19+Xiy+X2+X3. This is the highest chromosome number among Puerto Rican Dis- onychini. In closely related species with low and higher chromo- some numbers, high numbers tend to be associated with the



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Fig. 5. Karyogram of male D. comma. 2n=39(2X,y). existence of acro- or telocentric chromosomes (Robertson's rule), but in this species most chromosomes look metacentric and are capable of ring bivalent formation. The segregation to 22(3X) and 20(y) is confirmed by M IT (Fig, 3C and D). Karyogram (Virkki 1988b); 2n=44(6X) on females, 2n=42(3X,y) on males.
Oedionychina. This Pantropical subtribe has several Neotropi- cal genera cytologically characterized as follows: typically with 2n=22(X,y) and 10+X+y in males (Petitpierre et al. 1988), giant sex chromosomes segregating from a "distance bivalent" in male meiosis, 16 spztb, the lowest number known in Coleoptera, and very large spermatocyte I (Smith and Virkki 1978, Virkki 1985, Virkki and Denton 1987). Aggregation of nuclear pores to "nuclear



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19911 Virkki et al. 381
sieve complexes" (Virkki and Kimura 1978) in the growing sper- matocyte I characterizes Alagoasa spp. and many other Neotropi- cal genera formerly included in Oedionychus spp. (Virkki 1976). The inferred polarity (Stephens 1980) of the latter character points to Alagoasa and b'Oedionychus" as more derived than Ornophoita, which shows random distribution of nuclear pores in their spermatocyte I.
The orientation and segregation of the giant univalent sex chro- mosomes, as well as the growth of spermatocyte I in Oedionychina, have theoretical and phylogenetic implications (Smith and Virkki 1978, Virkki 1970, 1988a). Ornophoita cyanipennis cyanipennis (Fabricius) This oligophagous beetle feeds principally on the verbenaceans Clerodendrurn aculeaturn and Phyla nodiflora, especially on bor- ders of mangroves and other wetlands where the host plants are sympatric (Virkki 1980). It has a West Indian to southern North America distribution (Wilcox 1983). Puerto Rican samples are largely comprised of individuals with unicolored elytra; individu- als with white spots are rare (Virkki 1980). A spotted color morph 0. c. octornaculata (Crotch) prevails from Texas to Florida (U.S.A.), and perhaps on some of the other Caribbean islands (Blake 1931, Wilcox 1983).
Meiogram (Fig. 6A) and M I (Virkki 1979b): 10+X+y. Sper- matogonial metaphases show 2n=22(X,y) (Virkki 1979b). As found for many Ornophoita spp. (Virkki 1983), the Y chromosome is acrocentric or submetacentric, having, in contrast to X, unequal arms. Profiles of autosomal bivalents show all chromatids united by what may be a chiasma terminalized during a preceding diffuse diplotene, if not an original terminal contact. Cross or ring biva- lents have never been observed. Each chromatid shows a "tele- phone-handle" shape in the large bivalent closest to the sex chromosomes, but, where the free arm is short, it projects pole- wards leaving the centric gap equatorialwards from it. Jamaican samples of 0. c. octornaculata have the same karyotype as 0. c. cyanipennis from Puerto Rico (Virkki, unpubl.). Idiogram, based on measurements of A I1 chromosomes. Sex chromosomes assume nearly 53% of total karyotype length, all chromosomes are metacentric (Virkki 19790).



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Fig. 6. Meiogram of three Puerto Rican Oedionychina. 10+X+y. A. Omophoita cyanipennis. B. 0. albicollis. C. Alagoasa bicolor. Omophoita albicollis (Fabricius)
This beetle lives in drier habitats and it is more sporadically found than 0. c. cyanipennis. It has been found feeding of Stachy- tarpheta jamaicensis (Verbenaceae) near the air strip of Mona Island and in the abandoned military air strip at Tortuguero. Heliotropium indicum (Boraginaceae) is a secondary host (Virkki 1980).
Meiogram (Fig. 6B) and M I (Smith and Virkki 1978): 10+X+y. The Y chromosome has even more unequal arms than in 0. c. cya- nipennis. A desynaptic autosome pair depicted closest to the sex



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Fig. 7. Karyogram of A. bicolor. 2n=22(X,y).



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384 Psyche [vo~. 98
chromosomes (Fig. 6B) is often seen in Oedionychina from the Puerto Rico region. Because such univalents do not move to the poles but remain facing one another not far from the equator, they may show incipient distance pairing rather than asynapsis or precession.
Alagoasa bicolor (L.)
Compared to 0. c. cyanipennis and 0. albicollis, this is a seden- tary species that seldom leaves its host plant. It is sympatric with 0. c. cyanipennis, and it feeds on C. aculeaturn and Aegiphila mar- tinicensis (both Verbenaceae), the latter not associated with wet- lands. In spite of published records from other islands, the distribution of this species is probably limited to Puerto Rico and the Virgin Islands (Blake 1940). Some aspects of the life history, ecology, and behavior of this species in Puerto Rico have been studied (Virkki 1979a, 1980; Virkki and Zambrana 1980, 1983). Meiogram (Fig. 6C) and M I (Virkki 1970, 1989a): 10+X+y. Both sex chromosomes are nearly mediocentric, X slightly larger than Y. All autosomes look acro- or telocentric. Karyogram (Fig. 7) and spermatogonial mitosis (Virkki 1970): 2n=22(X,y). The autosomes, which have distal collochores (Virkki 1989a) in meiosis, do not show proximal collochores in these mitoses either, but their chromatids do not immediately open to stop at the final contact on the telomeres. There are some "sticky bridges" that slow down the separation of the chromatids. We have studied a sample taken from C. aculeaturn in Emmaus, St. John (United States Virgin Islands), that shows the same karyotype as the Puerto Rican sample.
Idiogram. The sex chromosomes comprise 52% of the total karyotype length, all autosomes are telocentric (M. Mojica 1990 pers. corn.). M I1 chromosomes are currently being studied. The cytological, hypothetical synapomorphic characters of Oedionychini (Disonychina and Oedionychina) are summarized in Fig. 8. It should be noted that a 10+X+y meioformula has appeared in Omophoita and in Alagoasa, constituting a parallelism. Also, the status of the nuclear pore distribution in Asphaera is uncertain (Virkki 1976); morphological characters (Scherer 1983) seem to



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386 Psyche [vo~. 98
support our hypothetical placement. Virkki (1970, 1988a) sug- gested that the evolution of these Disonychina and Oedionychina can be tracked to some genera related to Altica and Syphraea, the putative primitive "tribal groupings" Alticini and Hermaeophagini, where male meioformulae 11+X+y occur. It should be noted that the use of tribal names in the Alticinae is highly suspect and not well founded at this point (D. Furth 1991 pers. comm.). A common ancestor for Disonychina and Oedionychina should be looked for among relatively remote forms having karyotypes like those in Stenophyma sp., with unpaired, synorientated sex chromosomes of moderate size (Virkki 1970). A translocation of such a Y chromo- some on an autosorne would immediately produce a neo-system Xiy+X2, as found in Disonychina. Oedionychina would have evolved without such translocation, under enormous increase in the size of both sex chromosomes. It seems feasible that a simultane- ous increase of the spermatocyte size occurred in response to the increasing size of the Y chromosome, which has bands active in the diplotenic growth stage of spermatocyte I (Virkki and Denton 1987). Cell size and genome size increase have been positively correlated in succulent plants (De Rocher et al. 1990). Intraspe- cific variation of these parameters is similarly correlated in Tri- bolium (Coleoptera: Tenebrionidae), a genus showing spermatocytes of conventional size (Alvarez-Fuster, et al. 1991). Since the very large spermatocytes of Oedionychina would not fit in a cyst formed by only two or four cyst wall cells, alternative rearrangements became necessary: either to enlarge the cyst through additional cell growth or multiplication of the cyst wall cells, or to reduce the number of spermatocytes per cyst. The latter alternative was realized, in continuation of a trend already estab- lished on this inferred evolutionary lineage. Among the chromoso- mally most advanced Oedionychina are Asphaera spp., where distance sex multivalents occur (Petitpierre et al. 1988, Vidal 1984). These were usually noted X+ny (n=l-7), but since females became available for study, the X chromosome was found to be multiple: nx+Y (Virkki and Santiago-Blay, unpubl.). The multiple chromosomes are relatively small but of different size, suggesting a repeated sequence of centric fissions of formerly large chrorno- somes followed by pericentric inversions. Other advanced genera are Walterianella Bechynk, where autosomal centric fissions have



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19911 Virkki et al. 387
led to 22+X+y karyotypes (Petitpierre et al. 1988), and an unde- scribed Alagoasa with 5+X+Y due to autosomal centric fusions (Virkki and Santiago, unpubl.).
The chromosomal and cytological unorthodoxies of Oediony- chini, and especially of Oedionychina, warrant a comparative study of alleged related genera (see Seeno and Wilcox 1982, pp. 139-141), particularly the Old World Oedionychus. The Puerto Rican beetles of the tribe Oedionychini are cytologically typical of the inferred sister subtribes Disonychina and Oedionychina. In four Disonychina (Disonycha spilotrachela, D. comma, D. leptolineata, and D. eximia), metacentric autosomes prevail. Interspecific differences are expressed mainly in the diploid number, from 2n=30(4X) Q I 29(2X,y) 0 to 2n=44(6X) Q I 42(3X,y) 0. The sex chromosome association in male meiosis is either Xiy+X2 or Xiy+X2+X3. Disonycha leptolineata and D. comma are new records for Puerto Rico. In contrast, the three species of Oedionychina (Omophoita c. cyanipennis, 0. albicollis, Alagoasa bicolor), have 2n=22(X,y), with a simple distance sex bivalent in male meiosis (X+y). The interspecific differences are mainly due to a different centromere position. We suggest that karyotypes as those encountered in contemporary Stenophyma gave rise to Oedionychini by increase in size of sex chromosomes and/or by chromosomal rearrangements.
Los escarabajos puertorriquefios de la tribu Oedionychini son citologicamente tipicos de las subtribus hermanas inferidas Dis- onychina y Oedionychina. En cuatro Disonychina (Disonycha spi- lotrachela, D. comma, D. lepotolineata, y D. eximia), estudiadas, prevalecen 10s autosomas metackntricos. Las diferencias intere- specificas ocurren mayormente en el numero diploide, desde 2n=30(4X) Q I 29(2X,y) 0 hasta 2n=44(6X) Q I 42(3X,y) 0. La asociacih de cromosomas sexuales en la meiosis de 10s machos es X,y+X2 o Xiy+X2+X3. Disonycha leptolineata y D. comma son nuevos registros para Puerto Rico. Por contraste, las tres especies de Oedionychina (Omophoita c. cyanipennis, 0. albicollis,



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388 Psyche [vo~. 98
Alagoasa bicolor), tienen 2n=22(X7y), con un bivalente sexual de distancia sencillo en la meiosis del macho (X+y). Las diferencias interespecificas se deben mayormente a las deferencias en la posi- ci6n del centromero. Sugerimos que cariotipos como 10s encontra- dos en Stenophyma contemporineos originaron Oedionychini mediante el crecimiento de 10s cromosomas sexuales ylo las reor- denaciones cromos6micas.
ALVAREZ-FUSTER, A., C. JUAN, AND E. PETITPIERRE 1991. Genome size in Tribolium flour-beetles: inter- and intraspecific variation. Genet. Res. 58: 1-5.
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1933. Revision of the beetles of the genus Disonycha occurring in America North of Mexico. Proc. U. S. Natl. Mus. 82: 1-66. 1940. Oedionychis fasciata (Fabr.) and closely related species. Proc. Ento- mol. Soc. Wash. 42: 170-175.
1955. A revision of the vittate species of the chrysomelid genus Disonycha from the Americas south of the United States. Proc. U. S. Natl. Mus. 104: 1-86.
DE ROCHER, E. J., K. R. HARKINS, D. W. GALBRAITH AND H. J. BOHNERT 1990. Developmentally regulated systemic endopolyploidy in succulents with small genomes. Science 250: 99-101.
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1991. Selection tropique chez les Alticinae (Coleoptera: Chrysomelidae) suite. Bull. mens. soc. Linn. Lyon 60(2): 53-72. PETITPIERRE, E., C. SEGARRA, J. S. YADAV AND N. VIRKKI