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Chromosomal repatterning and linkage group conservation in mosquito karyotypic evolution.

Linkage group conservation has been a topic of considerable evolutionary interest since Muller (1940) first suggested that linkage elements corresponding to chromosome arms were conserved in Drosophila evolution. Muller proposed that ancestral Drosophila possessed a haploid karyotype of six chromosomes (Muller's elements, or arms, A-F). These elements remained essentially intact except for paracentric inversions, which altered gene arrangement, and centtic fusions, which created new combinations of arms. Subsequent studies supported Muller's original proposal. Included among these studies are comparisons of homologous morphological markers (Sturtevant and Novitsky 1941; Patterson and Stone 1952), enzyme linkage maps (Loukas, et al. 1979), chromosome pairing in interspecific hybrids (Throckmorton 1982; Krimbas and Loukas 1984), banding patterns in polytene chromosomes (Ashburner and Berendes 1978), and in situ hybridization (Whiting et al. 1989).

Foster et al. (1981) raised the study of dipteran chromosomal evolution to a higher phylogenetic level by comparing linkage maps (consisting primarily of morphological markers) of Drosophila, Musca (housefly), and Lucilia (blowfly). They observed that linkage groups corresponding to chromosome arms in Drosophila were homologous metacentric chromosomes in Lucilia cuprina and Musca domestica and reasoned that linkage group conservation was not restricted to Drosophila, but was characteristic of chromosomal evolution throughout the higher diptera. We show in the present study that linkage group conservation exists among diverse genera of lower diptera (mosquitoes) as well.

Many of the same approaches used to draw inferences concerning chromosomal evolution in Drosophila have been applied to mosquitoes (Rai 1963, 1966; Kitzmiller 1976; Munstermann 1981; Munstermann et al. 1982; Sherron and Rai 1984). Polytene chromosomes have been basic tools for interpreting chromosomal evolution in anopheline mosquitoes and other insects (simulids, chironomids, drosophilids). However, usable polytene chromosomes are not present in most culicine mosquitoes [exceptions are Orthopodornyia (Munstermann et al. 1985) and Sabethes (Munstermann and Marchi 1986)]. In the absence of good polytene chromosomes in culicine mosquitoes (Aedes and Culex), enzyme linkage maps have proven especially useful for studying karyotypic evolution. Biochemical loci are particularly well suited for identifying chromosomal homoiogies because these loci are more likely to be truly homologous than are morphological loci or chromosome bands.

In contrast to most insect groups, the chromosome number of culicine mosquitoes, consisting of approximately 2500 species, is essentially invariant (2N = 6) (Rai et al. 1982). Polytene chromosome studies in anopheline mosquitoes have indicated that despite the numerical uniformity extensive chromosomal repatterning has occurred in anopheline evolution (Kitzmiller 1976; Green 1982). In the absence of good polytene preparations in Aedes, early workers speculated that karyotypic evolution in this genus might be

qualitatively different than in anophelines, involving point and genic mutations rather than gross structural changes (Rai 1966). More recent comparative studies of aedine karyotypes have revealed evidence of structural changes similar to those in anophelines (Motara and Rai 1978; Munstermann 1981).

In this study, we have compared published enzyme linkage maps of six Aedes species and have identified structural changes and conserved linkages in Aedes chromosomes. We have also compared Aedes maps with enzyme maps of species of three other mosquito genera (Culex, Anopheles, and Toxorhynchites) and with Drosophila rnelanogaster.

AlEDES ENZYME MAPS AND

LINKAGE HOMOLOGIES

Maps of enzyme loci for six species groups in four subgenera of Aedes have been published.

Although they are not complete, and in some cases there is a dearth of data, they are sufficiently well developed to evaluate mosquito karyotypic evolution (tables 1, 2). Aedine mosquitoes typically have three homomorphic pairs of chromosomes with one pair shorter than the other two. The position of the centromere relative to enzyme loci has not been determined for any chromosome, but all chromosomes appear to be metacentric or nearly so (Rai et al. 1982). The Aedes aegypti karyotype and linkage map have traditionally been the standard in correlating linkage groups with chromosomes in other Aedes species (Munstermann 1981, 1990a). The shortest chromosome, designated LG I, carries the sex locus in A. aegypti and presumably other aedines (McDonald and Rai 1970). In A. aegypti, the enzyme loci, Me, Idhl, Acp, and Est2, are linked to the sex locus on linkage group I (LG I). Linkage group II includes Mdh2, Pgm, Gpd, Idh2, and Ldh. Associated on linkage group III are Sod, Gpi, Hk, Odh, and Pgd. Assignment of loci to LG II or LG III in other aedines is based on similarities of linkage associations to A. aegypti. To date, 15 loci have been mapped in at least two of the six Aedes species; we used these loci to make inferences about mosquito karyotypic evolution.

Subgenus Stegomyia

All homologous enzyme loci mapped in the three Stegornyia species appear to be conserved linkages in which both synteny and gene order have been retained (fig. 1). On LG I, Me and the sex locus, which are tightly linked, are centrally located in aegypti (and albopictus?) but terminally located in scutellaris. The relative positions and map distances of Pgm, Idh2, Gpd, and Est5, on LG II are nearly identical in all three species. These loci probably occupy one arm of chromosome two. Similarly, Gpi, Odh, Pgd, and Hk occupy the same relative positions of what may correspond to an arm of chromosome three. The only karyotypic changes suggested by map comparisons in the Stegomyia is a paracentric inversion on LG I converting the central position of Me and sex in aegypti to a terminal position in scutellaris.

Subgenera Stegomyia and Protomacleaya

Much of the linkage associations between A. aegypti (Stegomyia) and Aedes triseriatus (Protornacleaya) have been conserved (fig. 2). LG I appears to be relatively unchanged. Me, sex, and Idhl represent conserved linkages, because they reside on the same chromosome and their order is unchanged. Idhl is centrally located in aegypti but subterminal in triseriatus. Except for the inversion of Gpd and Idh2 in the Pgm-ldh2-GpdEst5 segment of LG II, this association of loci would also represent a conserved linkage. The Gpi-Odh-Hk segment of LG III of aegypti has been translocated to LG II of triseriatus and HkOdh inverted. Mdh2 on LG II of aegypti has been translocated to LG III of triseriatus (fig. 2).

Subgenus Finlaya

Except for Pgd and Xdh (Tadano 1988), all loci so far mapped in Aedes togoi (Subgenus Finlaya) are on the sex chromosome (LG I) (table 2). The sex-linked loci in A. togoi are distributed on all three linkage groups of the Stegomyia and on two linkage groups of the Protornacleaya (fig. 3). The togoi sex chromosome can be created from the Stegomyia karyotype by translocating the Gpi-Odh-Sod segment of aegypti LG III and the Pgrn-Idh2-Gpd-Est5 arm ofaegypti LG II to a small piece of the sex chromosome and including the sex locus and Acp (fig. 3A). Odh-Sod in the first segment and Idh2-Gpd in the second are inverted.

Even fewer changes (two whole-arm translocations) are required to create the togoi sex chromosome from triseriatus components. The togoi sex chromosome is essentially triseriatus chromosome two with the sex locus inserted in the middle (fig. 3B).

Subgenus Ochlerotatus

Despite the few loci mapped in Aedes atropalpus (Subgenus Ochlerotatus), some comparisons are possible. In atropalpus, Mdh and Pgd are linked to sex and Me is autosomal; the reverse is true in Stegomyia and Protomacleaya (table 2). Whereas a minimum of three to four translocations involving all linkage groups are required to create the differences between atropalpus and the Stegomyia species, only one or two are required for the atropalpus-triseriatus divergence. The association of Gpi and Idh2 on LG II of both atropalpus and triseriatus suggests the conservation of this segment in these two groups.

Summary of Aedes Chromosomal Changes

Interspecific comparisons of Aedes enzyme linkage maps have revealed that despite uniformity in karyotype number and gross morphology, Aedes chromosomes have been extensively modified. Translocations and inversions alone can account for the differences in location and arrangement of enzyme loci on the three linkage groups. Inversions have been common in regions corresponding to chromosome arms but occurred infrequently in the center of the linkage assembly. Because chromosomes in all Aedes species are metacentric or submetacentric, most inversions have necessarily been paracentric. This paracentricity is not surprising because inversions in a wide range of insects, including A nopheles (Green 1982), the Chironomidae (White 1978), and Simuliidae (Rothfels 1979), are paracentric rather than pericentric. White (1978) observed that in over 300 species of Drosophila, paracentric inversions were 200 times more common than pericentric.

Translocations in Aedes have also been common; however, to conserve the typical Aedes karyotype of three metacentric chromosomes, most translocations have been of the Robertsonian variety. The frequency of translocations in aedine chromosomal evolution appears elevated as in chironomids (aedines and chironomids belong to the suborder Orthorrhapha or lower diptera); in contrast, translocations in Drosophila (a member of the suborder Cyclorrhapha or higher diptera) have been rare (three translocations in 6400 structural changes in 300 species studied) (White 1978).

LINKAGE CONSERVATION IN MOSQUITOES

If most structural changes in Aedes chromosomes are the product of centromeric translocations and paracentric inversions, we would expect to find blocks of genes corresponding to intact chromosomal elements. Notable examples of such conserved groups of enzyme loci identified in our study include: (1) All linkage groups in the three Stegomyia species, (2) The Me-Sex-IdhlAat2 segment of the sex chromosome in Stegomyia and Protornacleaya, (3) The Gpi-Hk-Odh segment in all six Aedes species, and (4) The Pgm-Gpd-Had-ldh2 segment in all six Aedes species. These examples represent conserved linkages in which both synteny and gene order are conserved.

Enzyme maps for two species of Culex (C. piplens and C. tritaeniorhynchus), four species of Anopheles (A. albimanus, A. quadrimaculatus, A. culicifacies, and A. stephensi), and Toxorhynchites rutilis have been developed bringing to 13 the number of mosquito species for which enzyme maps are available (table 2). Comparison of the 13 enzyme maps permits tentative assignment of mosquito enzyme loci to chromosome elements sensu Muller (1940). As in Drosophila, the ancestral culicid karyotype appears to consist of six elements (arms?), designated A-F (table 3).

The sex locus is associated with loci on elements A and B in the three Stegomyia species and Aedes triseriatus, with elements D and F in Aedes atropalpus and with elements C and E in Aedes togoi. The data for sex linkage in the other genera are sparce, but several enzyme loci that are sex-linked in Aedes are also sex-linked in Culex and Anopheles. A good correlation exists in all mosquito species with respect to the loci associated with elements C and E. The only locus assignable to element D is Mdh; the remainder of the loci reside on element F.

If specific enzyme loci can be assigned to karyotypic segments corresponding to chromosome arms, then these loci can be used to identify the putative ancestral elements that have combined to form linkage groups in extant mosquito species (table 4).

To determine whether linkage homologies might extend to distantly related families within the diptera, we compared the culicid enzyme linkage map with that of Drosophila melanogaster (Collier 1990). Eight instances of conserved syntenies between higher and lower dipterans were identified (table 5).

DISCUSSION

Two conclusions were derived from a comparison of culicid linkage maps. The first is a reinforcement of previous observations that karyotype evolution in mosquitoes has involved several significant structural changes, mostly Robertsonian translocations and paracentric inversions. The second, and of more general significance, is the association of enzyme loci with linkage groups corresponding to chromosome arms and the conservation of these linkage groups during mosquito evolution. Comparisons were made at three levels: (1) interspecific within Aedes, (2) intergeneric within Culicidae, and (3) families within the lower and higher Diptera.

Several instances of linkage conservation were identified among the six species and four subgenera of Aedes. In some cases (e.g., Stegomyia species) the linkage arrangements point to conserved linkages in which both synteny and gene order have been maintained. In other cases, the loci are syntenic but gene order has not been conserved.

When linkage maps of Culex, Anopheles, and Toxorhynchites are compared with the Aedes maps, a more general picture of mosquito chromosomal evolution emerges. Linkage hornology between these culicid genera was sufficient to identify six syntenic arrangements of enzyme loci suggestive of ancestral linkage groups. To maintain the three metacentric chromosomes characteristic of culicids, most modifications in linkage associations during culicid evolution appear to have involved exchanges of entire arms. This model is generally supported by enzyme map comparisons as well as cytological evidence, but because centromere placement in culicids has not been definitively established, some caution should be observed in interpreting the conserved elements as chromosome arms. Each species or species group has its characteristic combinations of chromosome elements created by RobertsonJan exchanges. The loci within the linkage groups have been rearranged primarily by paracentric inversions. Examples of pericentric inversions, partial-arm translocations, or multiple translocation/inversion events were observed less frequently. As expected, increasing the phylogenetic distance between two groups increases the likelihood that conserved linkages have been converted to conserved syntenies by structural rearrangements.

Lower diptera (including mosquitoes, midges, and gnats) and higher diptera (including Drosophila and house flies) have been on separate evolutionary tracks for over 250 million yr. Comparisons of composite enzyme maps of mosquitoes with the Drosophila melanogaster enzyme linkage map suggests that several groups of enzyme loci have been conserved, although most traces of hornology between the two dipteran lineages have disappeared. These conserved linkages are found on all six mosquito chromosomal elements and on seven of the eight chromosomal arms of D. melanogaster.

Munstermann and Craig (1979) identified linkage homologies between Aedes aegypti and two Culex species and suggested that linkage associations can track chromosomal restructuring during the divergence of culicine species. Munstermann (1981) and Rai et al. (1982) summarized what was known about Aedes chromosomal evolution, including enzyme map homologies, and noted that transposition of blocks of linked enzyme loci, as well as numerous inversions, had occurred in the divergence of Aedes aegypt, Aedes triseriatus, and Aeries atropalpus. Hunt (1987) found that Pgm and a dieldrin-resistance locus, along with the Odh locus, were linked on the same chromosome arm in three Anopheles species, which is also the case in Aedes.

The phenomenon of linkage group conservation appears to be a common feature in the evolution of other eukaryotic groups. Leslie (1982) found linkage groups conserved in three genera of poeciliid fish, and Morizot (1983) found evidence of intact linkage groups extending over 400 million yr of vertebrate evolution from fish through amphibians to mammals. Mammalian groups in which karyotypic conservation has been found include Homo, Bos, Fells, Mus, and Peromyscus (O'Brien et al. 1980; O'Brien and Nash 1982; Dawson et al. 1983; Ohno 1983; Womack and Moll 1986; O'Brien et al. 1988). Leach and Howard (1987) described the conservation of linkage groups between an incompatibility locus and Gpi in five plant species.

Despite its apparent ubiquity in eukaryotes, the evolutionary significance of and the mechanisms that promote linkage group conservation have yet to be identified. Hilliker and TrusisCoulter (1987) have performed the most rigorous study to date attempting to identify the causes of this phenomenon. They hypothesized that linkage conservation is caused by structural constraints imposed by the arrangement of chromosome arms into domains during interphase of the cell cycle. However, their results did not support their hypothesis and they concluded that linkage group conservation results not from a single factor, but from several unidentified factors. Included among these are the following:

1. Functional interactions between linked loci (Ohno 1983); an example is housekeeping genes that share common regulatory elements (Farr and Goodfellow 1992)

2. Structural constraints imposed by overlapping genes transcribed on opposite DNA strands or by overlapping genes that use coding information from the same DNA sequence (Farr and Goodfellow 1992)

3. Genetic inertia imposed by segregational load and inbreeding associated with the establishment of newly arisen translocations and inversions (O'Brien and Nash 1982)

4. Constraints on the location of polymorphic versus monomorphic loci; polymorphic loci may be found together in linked segments more frequently than expected if the loci associate randomly (O'Brien and Nash 1982; Leslie 1982; Matthews and Craig 1989).

ACKNOWLEDGMENTS

Many of the background studies were completed at the Vector Biology Laboratory where research space was made available by the director, G. B. Craig. Financial support was provided by National Institutes of Health grants AI-02753 (to G.B.C.), AI-34521 (to L.E.M.), and the MacArthur Foundation's "Molecular Biology of Parasite Vectors" Program.

T. C. MATTHEWS[1] AND L. E. MUNSTERMANN [2]

[1]Department of Biology, Millikin University, Decatur, Illinois 62522

[2] Yale University School of Medicine, Department of Epidemiology & Public Health,

60 College Street, 606 LEPH, New Haven, Connecticut 06510

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