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Constitutive Heterochromatin Differentiation and Evolutionary Divergence of Karyotype in Oriental Anopheles (Cellia) 1

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Constitutive Heterochromatin Differentiation and Evolutionary Divergence of Karyotype in Oriental Anopheles (Cellia) 1 Pacific Science (1988), vol. 42, nos. 1-2 © 1988 by the University ofHawaii Press. All rights reserved Constitutive Heterochromatin Differentiation and Evolutionary Divergence of Karyotype in Oriental Anopheles (Cellia) 1 VISUT BAIMAI 2 ABSTRACT: Analysis of the mitotic karyotype of two clusters of closely re­ lated species of oriental Anopheles, the A . balabacensis and A. macula/us com­ plexes, has revealed interspecific differences in the amount and distribution of constitutive heterochromatin, particularly in sex chromosomes. Such a quali­ tative diagnosis of heterochromatin is useful in identification of these sibling species. The cytological evidence indicates a significant role of heterochromatin in chromosomal evolution of anopheline mosquitoes. The novel heterochro­ matin differentiation in sex chromosomes suggests an evolutionary role in the process of species divergence. Furthermore, extensive intraspecific variations of sex chromosome heterochromatin have been observed in natural popula­ tions of A . dirus A and B, while chromosomal rearrangement is very rare, if not absent. The gross heterochromatin variation may be correlated with variability in vectorial capacity, which may reflect its functional significance in coevolu­ tionary processes. CYTOLOGICAL VARIATION IS A general phe­ dipteran insects. Several authors working nomenon of the eukaryotic genome. Chromo­ with Drosophila (Carson and Yoon 1982, somal polymorphism usually persists in nat­ Carson et al. 1970, Stalker 1972), Chirono­ ural popul ations of higher organi sms in two midae (Ma rtin et al. 1974, Newman 1977), forms: chromosomal rearrangements and and Simuliidae (Bedo 1977) have discussed quantitative differences in constitutive hetero­ phylogenetic relationships among closely re­ chromatin. The former are well known in lated species groups through detailed investi­ man y groups of Diptera, and are believed to gation of chromosomal rearrangements. The have some adaptive significance in different application of this technique , based on com­ microenvironments (Dobzhansky 1970). The paratively fixed chromosome inversion and latter, on the other hand, although not un­ sex chromosome differences of unique arrays common in karyotypic evolution in many of chromosomal polymorphisms, is also use­ groups of eukaryotes (White 1973), is a form ful in the recognition of cryptic species of of polymorphism whose functional role and anophelines (Coluzzi and Kitzmiller 1975, implications in species differentiation remain Green 1982, Green and Miles 1980, Lambert unclear (Chang and Carson 1985, review by 1983, Saguna 1982, Subbarao et al. 1983). John and Miklos 1979). Constitutive heterochromatin is a general Detectable cytological differences are gen­ feature of the chromosome complement in erally useful in studies of taxonomy and eukaryotic karyotypes. The pericentromeric evolutionary relationships ofmany groups of heterochromatin can be readily demonstrated by C-band techniques (Arrighi and Hsu 1971). There have been numerous reports I This investigation received financial support from on the natural occurrence of quantitative the UNDP/World Bank/WHO Special Program for Re­ heterochromatin variation in both plants search and Training in Tropical Diseases, the U.S. and animals (e.g., Baverstock et al. 1982, Army Component (AF RIMS), and Mahidol University Fund . John 1981, John and King 1977, 1983, 2 Mahidd University, Department of Biology, Faculty Pathak et al. 1973, Patton and Sherwood of Science, Rama VI Road, Bangkok, Thailand 10400. 1982, Schweizer 1980, Weimarck 1975). Dif- 13 14 PACIFIC SCIENCE, Volume 42, January/July 1988 ferent degrees of staining intensity and differ­ chromosomes (2n = 6) with extensive hetero­ ent locations of constitutive heterochromatin chromatin variation. Kitzmiller (1976) listed apparently are due to different patterns of a total of only 30 species of Anopheles of C-bands. This has been a useful cytotaxo­ which metaphase karyotype descriptions or nomic technique (White 1978). Of particular figures had been demonstrated. More re­ interest, detectable heterochromatin dif­ cently, there have been some reports dealing ferences may provide a useful criterion for with inter- and intraspecific variation of sex identification of closely related species, for chromosome heterochromatin (Baimai et aI. example, in Drosophila (Baimai and Ahearn 1984a, Bonaccorsi et al. 1980, Gatti et al. 1978, Baimai et al. 1983). Recently, this 1977,Green et al. 1985, Vasantha et al. 1982, C-band method for detecting heterochromatin Wibowo et al. 1984). differences together with new fluorescence Comparative studies on karyotype analy­ techniques have been used successfully in sis of constitutive heterochromatin and chro­ separating certain cryptic species of Anopheles mosomal rearrangements thus offer a prom­ (Baimai et al. 1981,Gatti et al. 1977,Vasantha ising opportunity to explore the implications et al. 1982,Wibowo et al. 1984).Thus, hetero­ of natural chromosomal variation for a bet­ chromatin variation in natural populations ter understanding of the microevolutionary is of special interest as a model for examining process of oriental anophelines. This paper its possible role in evolutionary divergence at summarizes the cytological observations in the genomic level. some Anopheles species groups that suggest From the evolutionary genetics point of the evolutionary role of heterochromatin view, anopheline mosquitoes are one of the differentiation and briefly outlines some most interesting groups of the oriental fauna . of its implications in the epidemiology of Some of the Anopheles species groups play human malarial parasites. very important roles in transmission of human pathogens in the tropical region. Of the genus Anopheles, subgenera Anopheles SERIES NEOMYZOMYIA and Cellia are the most predominant groups , . each with some 200 known species (Harrison A focal point of attention is the leucosphy­ and Scanlon 1975, Rao 1984, Reid 1968). rus species group, belonging to the Neomy­ Some of these described species have re­ zomyia series of the subgenus Cellia, since ceived close attention for detailed investiga­ most of its species members, especially the tion because they serve as important vectors Anopheles balabacensis complex, are primary for human malarial parasites. Naturally, vectors of human malarial parasites in their much of the genetic studies of anopheline particular areas of distribution. This species mosquitoes have been made mainly as applied complex is exclusively a forest and foothills field researches on relatively few species of group, and is widely distributed throughout medical importance (Coluzzi and Kitzmiller the oriental region ranging from India 1975, Kitzmiller 1976, White 1980). Little (Assam) through all countries in Southeast work has been done broadly in terms of evo­ Asia, Taiwan, and the southern part of the lutionary biology. Like all other dipterans, Republic of China (Figure 1). Early sys­ information on chromosomal polymorphism tematic studies of this species complex of anophelines is best known from studies of showed a wide range of geographical and chromosomal rearrangements as seen in the morphological variation (Colless 1956, Reid polytene chromosomes prepared from larval 1968). Recently recognized species of the salivary glands or ovarian nurse cells of half­ A . balabacensis complex include A. balaba­ gravid females (Coluzzi et al. 1979, Green censis, sensu stricto from Sabah and the 1982, Kitzmiller et al. 1973). In contrast, less Philippines, A. takasagoensis from Taiwan, emphasis has been made with regard to the and A. dirus from Thailand (Peyton and Har­ analysis of metaphase karyotype of an­ rison 1979, 1980). The results of cytogenetic ophelines in spite of its small number of studies of these species showed that they Differentiation and Divergence in Oriental Anopheles- BAIMA I 15 ~ dirusA ~~APAN \ ~ ~ I I I " . / n m XY " mil takasagoensis . ~ J ' - ' ,.,, '.... INDIA .1! ' ;;;i~~ :~ II :: nHDr HXY ~ nPHILIPPINES IV ~~ TNA M ~ § balabacensis I Dr XY KAMPUCHEA ,'1;,] . '", ~ ';'.Y~::::/ ~ ~ ~ dirus C i F ·~_.~..... ~ i. SABAH ~ .. .~ ~~IBI fd 'to X Y nH m HX y ? "'JAVA ~s~~ , ~ :••.. ~~~ '0" ~ B dirusB ~oo~~-p~ '. ," . INDONESTA ,f .. ~ I HDr XY AUSTRALIA n F IGURE I. Distributions of the six species of the Anopheles balabacensis compl ex in Southeast Asia, depict ed with diagrammatic representati ons of mitot ic chro moso mes using Giemsa staining. Heterochromatin is indicated in black or shaded. were distinct biological species (Baimai et al. easily by chromosomal analyses. In addition, 1981 , Hii 1982). However, Kanda et al. species members of the A . balabacensis com­ (1981, 1983) have suggested that the strain s plex have different geographical distributions of " A. balabacensis" from Thailand, pen­ (Table 1, Figures I, 2). Anopheles balabacensis insular Malaysia, and Sabah represent three is restricted to Sabah , East Kalimantan, and subspecies of this species complex. Detailed Palawan, while A. takasagoensis has been taxonomic studies (Peyton and Harrison, per­ recorded only from Taiwan. Members within sonal communication) together with cyto­ the taxon A . dirus have been found on the genetic analysis of natural populations of mainland of Southeast Asia. It is interesting A. dirus (Baimai et al. 1984b, 1987) have re­ to note that A. dirus D is relatively wide­ vealed that it is actually a cluster of at least spread in western Thailand, occurring in sym­ four closely related species provisionally
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