Chromosomal Variability in the Antarctic , (Diptera: )

WILLIAM R. ATCHLEY2 AND BRENT L. DAVIS3 ABSTRACT Ann. Entomol. Soc. Am. 72: 246-252 (1979) Chromosomal inversion polymorphism is examined in the Jacobs (Diptera: Chironomidae). This insect is the southernmost free-living holometabolous species and is restricted to ca. a 650-km range on western side of the Antarctic Peninsula. B. antarc- tica is a diploid species with a chromosome complement of 2n=6. Five chromosomal inver- sions were found among ca. 1200 from 18 localities. One inversion is sex-linked. Two inversions exhibited highly significant interpopulational differentiation in the frequency of inversion heterozygotes. Attempts to correlate inversion heterozygosity with several en- vironmental variables including ecological complexity and 3 soil variables, i.e., pH, electri-

cal conductivity and percent organic material, gave non-significant results. Several hy- Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 potheses are advanced to explain the observed patterns of genetic variability.

Virtually nothing is known about genetic variability area can be found in Strong (1967), Peckham (1971) and in the terrestrial insect fauna of Antarctica. The species references therein. of Antarctic insect most suitable for genetic analyses is All specimens examined in this study were mature lar- the wingless midge, Belgica antarctica Jacobs (Diptera: vae preserved in 3:1 ethyl alcohol - acetic acid fixative. Chironomidae), which is the southernmost free-living The sex of these individuals was determined by the gen- holometabolous insect. This monotypic genus is re- ital analagen method (Wiilker and Gotz 1968). Cytolog- stricted to ca. 650-km range from Elephant Island in the ical preparations were made by dissecting out the sali- northern sector of the South Shetland Islands through the vary glands into 60% proprionic acid, staining with Gerlache Straits of the Palmer Archipelago and south to lacto-proprionic-orecin and squashing in 60% proprionic 65° 27' south latitude in the Argentine Islands on the acid. western side of the Antarctic Peninsula (Wirth and Gres- sitt 1967). The mammal and bird species occurring in the Ant- Biology of Belgica arctic are considered to be either transient or marine and Preliminary studies on the biology of Belgica antarc- the terrestrial fauna includes Acarina, Collem- tica have been made by Torres (1953), Strong (1967) bola, Mallophaga, Anoplura, Siphonaptera as well as and Peckham (1971). Larval habitats include moist soil Belgica antarctica (Gressitt 1967). Since holometaboly under rocks, association with the nitrophilous alga Pra- is a derived trait in , B. antarctica would be siola, in mosses and in the rhizospheres of the grass assumed the evolutionarily most advanced free-living Deschampsia antarctica Hook. f. The larvae are not terrestrial Antarctic . found in association with free water. More detailed in- In this study we explore 2 themes. First, we provide formation on the larval habitats can be found in Peckham preliminary data on the chromosomal cytology of B. (1971). antarctica and explore the role of inversion heterozygos- Oviposition occurs in damp moss or similar substrate ity in adapting this species to a polar environment. Sec- with ca. 30-50 eggs laid in a gelatinous mass per ovi- ond, we examine interpopulational variation in inversion position. Hatching occurs in ca. 10 days followed by heterozygosity in a series of island populations off the dispersal of the larvae into the larval media. Individual Antarctic Peninsula. females have been observed to oviposit only once and Materials and Methods parthenogenesis is not known. Larval food appears varied consisting of dead plant A total of 1182 individuals was collected from 18 material, fungal hyphae, algae, and moss. Limited data localities on 10 small islands off the south coast of An- from Peckham (1971) indicate a preference for algae vers Island in the vicinity of Arthur Harbor (64° 46' S, over moss. 64° 02' W) on the Antarctic Peninsula. All collections Peckham (1971) has hypothesized 6 rather than the were made during the austral summer of 1974-1975 usual 4 larval instars infl. antarctica based on frequency and each sample represents a single collection. These distributions of larval head capsule length. There is also localities are described in Table 1 together with a local- some evidence that the life cycle lasts for > 1 yr in less ity code and are shown in Fig. 1. The total distance be- favorable habitats but more than one generation per year tween extreme samples (excluding EA1) was ca. 7 km. can occur in highly favorable habitats. This point re- An arrow and dollar sign denote the site of the United quires further clarification. States National Science Foundation Field Station. De- Mobility in adults is limited as a result of the loss of tailed information on the ecology of the Arthur Harbor wings and mating occurs on the substrate. Dispersal over any distance is passive involving air currents, transport 1 Received for publication Sept. 5. 1978. in the nesting materials of birds, etc. B. antarctica often 1 Dept. of Entomology. Univ. of Wisconsin. Madison 53706. 3 Dept. of Biol. Sciences. Texas Tech Univ.. Lubbock 79409. occurs in clumps of Deschampsia, moss or non-living 246 ©1979 Entomological Society of America 0013-8746/79/0202-4607$00.75/0 March 1979] ATCHLEY AND DAVIS: Belgica CHROMOSOMAL VARIABILITY 247 Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021

Fie. 1.—Map of Arthur Harbor vicinity showing location of sampling sites. Insert shows the position of Anvers Island on the Antarctic Pennisula. Sample EA1 is not shown on this map. Table 1 provides an explanation of the locality codes.

Table 1.—Localities, locality codes, sample sizes, frequencies of inversion heterozygotes and ecological complexity values for 18 samples of Belgica antarctica Jacobs. Total sample size and average heterozygote frequencies are given at the bottom of each column. See text for clarification of symbols.

1 2 3 4 5 6 7 8 9 10 Locality A+B+ Ecological code Locality N A B C A+B A+C B+C C '%H 1-R complexity AAI Cormorant Island 58 0.379 0.224 0.069 0.121 0.017 0.000 0.000 0.534 0.063 3 ACI Limitrophe Island 66 .439 .394 .073 .091 .030 .015 .015 .742 .083 3 AEI Hermit Island 63 .444 .492 .254 .175 .063 .063 .111 .730 .124 1 AFI Ikes Island 44 .523 .409 .136 .183 .068 .045 .000 .773 .100 3 AGI Shortcut Island 49 .571 .367 .061 .204 .020 .041 .000 .735 .091 1 AG2 Shortcut Island 77 .571 .377 .078 .195 .039 .013 .026 .727 .094 1 AJI Bonapart Point 93 .613 .247 .000 .129 .000 .000 .000 .731 .072 4 AJ3 Bonapart Point 82 .524 .317 .061 .207 .037 .000 .012 .634 .082 4 AJ4 Bonapart Point 64 .531 .438 .047 .172 .000 .000 .016 .813 .091 3 AMI Norsal Point 55 .618 .200 .200 .091 .109 .036 .018 .745 .101 1 AM5 Norsal Point 72 .542 .306 .431 .139 .139 .069 .042 .847 .139 5 AM6 Norsal Point 68 .529 .235 .000 .118 .000 .000 .000 .647 .068 4 AO1 Litchfield Island 70 .514 .443 .314 .186 .071 .086 .086 .757 .126 3 AO4 Litchfield Island 66 .530 .288 .121 .167 .061 .015 .015 .667 .089 4 AO5 Litchfield Island 62 .452 .500 .258 .161 .048 .048 .048 .855 .118 2 AO6 Litchfield Island 101 .505 .535 .020 .287 .000 .020 .000 .762 .092 3 API Strandtmann Island 43 .419 .512 .372 .140 .116 .070 .047 .884 .140 2 EAI Port Lockroy 49 .551 .592 .041 .306 .000 .000 .000 .878 .105 2 1182 0.518 0.378 0.132 0.173 0.042 0.028 0.024 0.743 0.099 248 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA [Vol. 72, no. 2 debris which serves as nest material for several species One large inversion was found in chromosome I in of Antarctic birds. this study. It occurred from just mesad of the Balbiani Cytology ring to within a few bands of the other end of the chro- mosome and therefore encompassed the nucleolar or- B. antarctica is a diploid, sexually reproducing spe- ganizing region. Only 1 individual was found to be het- cies and, like many species of chironomids, has polytene erozygous for this inversion in this study but this is salivary gland chromosomes. However, the polytene apparently the same inversion which Martin (1962) found chromosomes are much smaller and more difficult to at a frequency of ca. 8% in the single population he study than many of the commonly examined species. B. examined. The latter population occurred at a consider- antarctica has a chromosome complement of 2n=6 with able distance from those included in this study. homologues tightly synapsed. A typical salivary gland Chromosome II (Fig. 2, 3a, c) can be distinguished cell from a female individual is shown in Fig. 2. While by a medially located puff containing a nucleolar organ-

the basic chromosome number in Chironominae is 2n=8 izer and be a darkly staining sub-terminal band seen at Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 (Martin et al. 1974), 2n=6 is apparently the basic chro- the bottom of Fig. 3a. For descriptive purposes, we have mosome number in the Orthocladiinae (Bauer and Beer- designated that portion of chromosome II with the sub- man 1952). terminal dark band as the left terminus and the other end Our studies have shown the occurrence of 5 chromo- as the right terminus. somal inversions in the populations examined thus far. Chromosome II has 2 large inversions which are het- The individual chromosomes and their respective inver- erozygous at high frequencies. Inversion A, with ap- sions can be described as follows. proximate breakpoints shown in Fig. 3a, occupies ca. Chromosome I is the shortest in the complement and 27% of the chromosome and ca. 9.5% of the total gen- can be recognized by a large Balbiani ring occurring ca. ome. Of the 1182 individuals we examined, 51.8% VA the distance from one end (Fig. 2, 3e). Further, it has were heterozygous for inversion A. Inversion B on chro- a large submedian puff containing a nucleolar organizing mosome II takes up ca. 23% of the chromosome and region. The chromosome end nearest to the Balbiani ring roughly 8.2% of the entire . Of all individuals is designated as the left end. examined 37.8% were heterozygous for B. The approx- imate breakpoints for B are given in Fig. 3a. Chromosome III is the longest chromosome of the complement and has a subterminal puff which also con- tains a nucleolar organizer (Fig. 2, 3b, d). We designate that chromosome end nearest the puff as the left termi- nus. This chromosome lacks any darkly staining subter- minal bands such as seen on chromosome II. Ill *•<, Two inversions occur in III. Inversion C occupies ca. 36% of the chromosome and ca. 13.6% of the total gen- i ome. It was heterozygous in 13.2% of all individuals examined and its breakpoints are shown in Fig. 3d. In- version D, which occurs ca. in the middle of the chro- mosome, is sex-linked and always heterozygous in the males. FIG. 2.—Typical salivary gland cell from a female of Belgica Chromosome II and III seem to be remarkedly devoid antarctica Jacobs showing the 2n = 6 chromosome comple- of reliable cytological landmarks. Only the position of ment.

c o B II II

B NO Vi ^ m NO »

A A

# c d \ I NO in ^' b ?• NO H0<2i • **

''* -"?

FIG. 3.—Individual chromosomes and approximate inversion breakpoints. NO = nucleolar organizing region and BR Balbiani ring. See text for further explanation. March 1979] ATCHLEY AND DAVIS: Belgica CHROMOSOMAL VARIABILITY 249 the puffs containing the nucleolar organizers, the darkly out by locality. In all cases, nonsignificant results were staining subterminal band on II and inversion D will re- obtained indicating no association between the hetero- liably distinguish the 2 chromosomes. zygotes of the various inversions. While the heterozygotes of the various inversions The Brandt-Snedecor procedure (Snedecor 1956, p. could be easily distinguished in the tightly synapsed 228) was employed to determine if statistically signifi- chromosomes, the absence of distinguishing features on cant differences in the proportions of inversion hetero- chromosomes II and III and the small size of the poly- zygotes occurred between samples. If the overall test of tene chromosomes made it impossible to identify the the 18 samples was statistically significant, testing was homozygous sequences of the 3 non-sexlinked inver- continued in a step-wise manner to ascertain the homo- sions with any accuracy. However, since we are inter- geneous subsets of samples. The elucidation of homo- ested in the relationships between chromosomal hetero- geneous subsets of samples is necessary to determine if zygosity and adaptive strategies, the inability to interpopulational differentiation has followed some ex-

distinguish inversion homozygotes is of little conse- plainable pattern, e.g., ecological gradients, dispersal Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 quence. patterns, etc. This statistical approach is analogous to Chromosomal Polymorphisms the protected least significant difference procedure of multiple comparisons testing recommended by Carmer Table 1 describes the sample sizes and the extent of and Swanson (1973). Each homogeneous subset is max- inversion heterozygosity by locality. The sample size (n) imal in that the addition of another sample gives a sig- at each locality is given together with the proportion of nificant chi-square value. individuals heterozygous for inversions A, B, C, A+B, In the case of inversion C, 2 samples had no hetero- A+C, B + C, A+B + C, the proportion of individuals zygotes and no general statistical rules exist for hypoth- heterozygous for one or more inversions (% H) and the esis testing when one or more group has a proportion of proportion of the total genome tied up in inversion het- zero. Therefore, in this case, a "biological" approach erozygotes (defined as 1 -R where R represents the amount was employed and these samples were considered to be of the chromosome available for free recombination, statistically homogeneous with the next sample in the i.e., uninvolved in the inversion). sequence which had 2% heterozygotes. This approach The varied diet of B. antarctica larvae together with assumes that heterozygotes in the 2 samples were rare the food preference data suggest a possible biological and simply not obtained in 2 localities due to sampling relationship may exist between variability and the num- error. Since the frequencies of the various inversions are ber of plant species in the larval habitat. Therefore, the statistically independent, delimitation of homogeneous final column in Table 1 provides a simple code for each subsets for heterozygotes of A+C, B + C, and A+B + C, sample which approximates the ecological complexity at was not attempted. that locality. Complexity was coded from 1-5 as fol- In the case of heterozygosity for inversion A, no sig- lows: 1—damp soil with no visible green vegetation; nificant differences were noted among the 18 samples 2 2—detritus with the large microscopic algae (X S = 16.94, P >0.25). However, highly significant crispa (Light f.) Menegh.; 3—Prasiola with scattered intersample differences were noted for inversions B and 2 2 clumplets of moss; 4—large moss beds or moss with C(forB,X s = 64.86,/>>0.001; for C, X S = 171.00, some grass; and 5—pure strands of the grass Deschamp- P <0.001). sia antarctica Hook. f. The last classification reflects Table 2 provides the homogeneous subsets of samples the climax community on the islands in the Arthur Har- for inversions B and C. With inversion B, there are 7 bor area. homogeneous subsets among the 18 samples and the This classification (with a single exception) also ap- pattern of subsets is the typical series of overlapping sets proximates the number of plant species at each location. indicative of clinal variation. In the case of inversion C, All values are off 1 number (i.e., code 1 has 0 plant 4 homogeneous subsets were detected. species, code 2 has 1 plant species, etc.,) except for the A clear biological interpretation of the patterns of var- case of category 5. In the latter case, the number of plant iability in inversion heterozygosity is not obvious from species is 1 but there is only a single locality (AM5) in the statistical analyses of the individual inversions. this category. Please note that the number associated Therefore, we examined chromosomal variability in a with each locality code identifies a particular sample and multivariate sense to determine if clustering of the sam- is not an ecological complexity value. ples would occur when all of the chromosomal data were In addition to information on ecological complexity considered simultaneously. The 17 samples from the im- of each site, data on soil pH, percent organic material mediate vicinity of Arthur Harbor (EA1 omitted) were and electrical conductivity were available for many sam- ordinated £y non-metric multidimensional scaling ples. Peckham (1971) indicated that the distribution and (Kruskal 1964) into 2-dimensional graphic representa- density of B. antarctica larvae was correlated with var- tion of the original Euclidean distance matrix. ious chemical aspects of the soil including pH, organic The data for the distance matrix consisted of the in- nitrogen, as well as certain chemical elements. version frequencies and are given in Table I. Originally, Except for the case of inversion D, no significant sex all the genetic data (column 2 - 10) in Table 1 were differences were noted for the various inversions and ordinated but the results were almost identical with those therefore the sexes were pooled for these analyses. In- obtained for a subset of the data (column 2-6). Because version D is sex-linked and always heterozygous in of the ease in interpretation of the ordination of the latter males. A series of chi-square tests of independence for subset of variables, we have presented these results in the heterozygotes of the various inversions were carried Fig. 4. 250 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA [Vol. 72, no. 2 plexity values of 3. The most aberrant sample in the or- dination was AM5 and it was the only sample where the complexity was scored as 5. In view of these results, we tested the hypothesis of a statistical relationship between ecological complexity and geographic position on the one hand and chromo- somal inversion heterozygosity on the other. All of the genetic variables from Table 1 were employed as one set of variables. The other set of variables comprised the ecological complexity code and the geographic position of the sample as represented as a series of cartesian co-

10.5- ordinates. The cartesian coordinates were obtained as

simply the distance from a specific latitude and longi- Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 tude reading so the X was the distance along a latitude scale and Y was the distance on the longitude scale. The 2 sets of variables were related by canonical cor- relation analysis (Morrison 1967). One eigenvalue was significant (P <0.01) and the corresponding eigenvector (Table 3) depicted a statistical relationship between the percent of the genome tied up in inversion heterozygotes and heterozygosity for inversions C, A and A+C on the one hand and the geographic coordinates on the other. The canonial coefficients for geographic coordinates were negative, indicating an inverse relationship be- tween geographic position and 1 - R and A+C and a II direct relationship with A and C heterozygosity. FIG. 4.—Two-dimensional ordination by non-metric multi- No significant relationship was noted between inver- dimensional scaling of inversion heterozygote frequencies from sion heterozygosity and ecological complexity in the 17 samples of Belgica antarctica. Samples are linked by small- canonical correlation analysis. Further, consideration of est pairwise Euclidean distance values. Explanation of locality the bivariate Pearson product-moment correlation coef- codes given in Table 1. ficients between ecological complexity and each of ge- netic variables gave statistically nonsignificant results in A distortion or "stress" of ca. 10% occurred be- each instance. There was also no statistical relationship tween the original distance matrix and the 2-dimensional between number of plant species at a locality and the plot. Therefore, to insure fidelity with the original dis- amount of inversion heterozygosity. Three soil variables tance matrix, the various samples were linked by the including percent organic matter, soil pH and electrical smallest pair-wise Euclidean distances based on the 5 conductivity were available from 7 localities. Statistical genetic variables. testing indicated no significant association between var- The ordination gives basically 3 clusters of samples iability in these soil characteristics and heterozygosity with 1 or 2 outlying samples. Axis I depicts a strong for the various inversion sequences. gradient for heterozygosity in inversion C and J - R, the latter being a measure of the amount of the genome tied Discussion up in inversion heterzoygotes. Thus, those samples with highest inversion C heterozygosity in order of decreas- A current vogue in population biology is to try and ing magnitude were AM5, API, AO1, AO5, AE1, and relate adaptive strategies or genetic variability in tem- AMI while AJ1 and AM6 had the lowest frequencies perate and tropical organisms to ecological stability and followed by AO6, AJ4, AJ3, AG1, AA1, and AC1. species diversity theory. Unfortunately, little informa- With regard to the amount of the total genome tied up in tion has been available for polar organisms. The polar inversion heterozygotes, API, AM5, AO1, AE1, and regions have often been described as "simple" ecolog- AO5 had the most while AA1, AM6, AJ1, AJ3 and AC1 ical systems although a better terminology might be to had the least. call these low species diversity systems. However, clas- Axis II depicts variation in inversion B heterozygos- sifying these areas as simple or low diversity ecosystems ity. AO6, API, AO5, AE1, AO1, and AJ4 had the high- obscures a distinction which is of paramount importance est frequencies while AM6, AA1, AMI, AO4, AM5, to the genetic basis of . According to Slobod- and AJ3 had the lowest frequencies. kin and Sanders (1969), low-diversity environments fall Superficially, it would seem from the ordination that in 3 general categories: (1) new environments in the pro- some correspondence exists between chromosomal het- cess of colonization; (2) "severe" environments that erozygosity and ecological complexity since samples could become abiotic with relatively slight environmen- AM6 and AJ1 had values of 4 on the complexity scale tal change; and (3) "unpredictable" environments where while samples AMI, AO5, AE1, AO1 and API had val- the variation in the environmental parameters is high and ues of 1 or 2. Except for samples AG1 and AG2 (with unpredictable both spatially and temporally. The optimal values of 1) and AO4 and AJ3 (with values of 4), the mechanism for adaptation will be largely determined by remaining samples in the intermediate cluster had com- which of these three categories prevails. March 1979] ATCHLEY AND DAVIS: Belgica CHROMOSOMAL VARIABILITY 251

If the environment is unpredictable over periods of time and other similar modifications appear commonly time greater than the length of a generation, little genetic in Arctic insects (Downes 1965, Byers 1969). tracking of the critical environmental parameters can oc- Consider now some of the features which have oc- cur. Consequently, we might expect the organisms to curred in B. antarctica as a possible adaptation to an have low amounts of additive genetic variance and to be Antarctic existence. highly "buffered" to stabilize morphogenesis in order With regard to inversion polymorphism, over 74% of that the organism can survive in the face of a high the almost 1200 individuals examined in this study were amount of random environmental variation. (By buffer- heterozygous for at least one inversion. Inversion A, ing, we mean any mechanism that retards phenotypic which occupies almost 10% of the total genome, is het- change in the face of environmental variability). erozygous at a frequency of almost 52% in the 18 sam- Conversely, if the environment is predictable and ples. Two other inversions, B and C, are heterozygous therefore characterized by considerable autocorrelation, at lower but still high levels in the various populations.

the need for extensive buffering would be considerably Inversion heterozygotes prevent reproduction by ga- Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 lessened. Even when the environment is severe (sensu metes in which 2-strand single crossovers have occurred Slobodkin and Sanders 1969), if there is autocorrelation within the inversion. Barring 2-strand double crossovers there may not be as much need for buffering as in an within the inversions, individuals with the simultaneous unpredictable system. occurrence of heterozygotes in A and B have no recom- Several authors (see Downes 1965 for review) have bination in ca. 17% of the entire genome. Inversions A suggested that the Arctic environment is highly variable and B simultaneously are heterozygous in slightly more and therefore genetic systems tend to be highly buffered than 17% of all individuals. When A, B, and C are si- with selection favoring those mechanisms which pro- multaneously heterozygous they tie up ca. 31% of the mote heterozygosity and reduce recombination. Some genome and this occurs in ca. 2.4% of all individuals. evidence exists to support this heterotic buffering hy- Table 1 indicates that, in toto, an avg of 10% of the pothesis in certain Arctic forms with chromosomal rear- genome is tied up in inversion heterozygotes in the 18 rangements, polyploidy and parthenogenesis being the populations examined. Thus, without selection for de- mechanisms for fixation of heterozygosity and reduction creased frequency of meiotic crossing over, inversion of recombination. Basrur and Rothfels (1959), for ex- heterozygosity would effectively reduce the amount of ample, found that several species of Arctic blackflies the genome where reproductively meaningful recombi- were highly heterozygous for chromosomal inversions nation could occur. as well as parthenogenetic and triploid. The occurrence of high levels of inversion heterozy- In addition to purely genetic mechanisms, morpho- gosity has been commonly assumed to be adaptive in logical and physiological modifications occur such as tropical and temperate Diptera in that some inversions loss of wings which would tend to produce "island" are significantly more frequent than others in certain type populations where little outcrossing occurs. Fur- ecological situations (Dobzhansky 1970, White 1973). ther, it has been hypothesized that longer generation Examination of the data on variation in percentage of the time would occur in polar insects. Whether this would various inversion heterozygotes in B. antarctica would result from selection or simply from lower avg temper- seem to follow this pattern since highly significant dif- atures is unclear. Whatever the cause it would increase ferences occur between ecologically divergent samples the time interval in which mutation and recombination in the described inversion sequences. However, univar- would operate, i.e., the same rates simply spread over a iate and multivariate statistical analyses indicate that no longer generation time. Wing loss, prolonged generation linear statistical relationship existed between inversion heterozygosity and a number of ecological parameters considered either singly or in combination (Tables 2, 3, Table 2.—Multiple comparisons testing for heterozygote Fig. 4). In particular, there was no relationship between frequencies for inversions B and C. Statistically homogene- ous subsets are connected by a line. chromosomal heterozygosity and either the degree of

Inversion B Inversion C Table 3.—Variables and canonical coefficients from a canonical correlation analysis. The canonical correlation AMI AM6 coefficient was 0.977. AA1 AJ1 AM6 AO6 Variable Coefficient AJ1 EAI AJ4 AO4 %H 0.431 AM5 AJ3 1-R 1.394 AJ3 AG1 A -0.856 AG1 AA1 B -0.249 AG2 AC1 Set 1 C -1.179 AC1 AG2 AB 0.370 AF1 AO4 AC 0.657 AJ4 AF1 BC -0.204 AOI AMI ABC 0.147 AEI AEI AO5 AO5 AF1 AOI X -1.603 AO6 API Set 2 Y -1.397 EAI AM5 Complexity -0.225 252 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA [Vol. 72, no. 2 ecological complexity at each locality or certain seem- Acknowledgment ingly relevant soil variables. Several explanations are possible for these results. We are indebted to our colleague, Larry R. Hilburn, First, the "correct" ecological parameters were not for his assistance throughout the project. James F. Crow, selected in the canonical correlation analyses. Thus, J. A. Downes, and Jon Martin made many helpful com- while there may be an ecological explanation for the var- ments on the manuscript. This research was supported iability in inversion frequencies, the relevant parameters by the National Science Foundation (OPP72-00475) and have not been uncovered. the National Institutes of Health (5-T32-GM07131). Second, there have been significant pertubations of some of the habitats in the very recent past so that our REFERENCES CITED designation of specific values for ecological complexity Basrur, V. R., and K. H. Rothfels. 1959. Triploidy in natural are unrealistic. We are aware of several instances where populations of the black Cnephia mutata (Malloch). Can. J. Zool. 37: 517-89. one or more elephant seals greatly altered the habitat at Downloaded from https://academic.oup.com/aesa/article/72/2/246/125422 by guest on 01 October 2021 a particular locality over a short period of time. Since Bauer, H., and W. Beermann. 1952. The chromosome cycle of the Orthocladiines (, Diptera). Zeits. Natur- the rate of ecological recovery is much lower in the Ant- forschung. 76: 557-89. arctic, due to the fragile nature of the Antarctic ecosys- Byers, G. W. 1969. Evolution of wing reduction in crane tem, some of our complexity values may not reflect the (Diptera: Tipulidae). Evolution 23: 346-54. ecological complexity as it existed a year or more before Carmer, S. G., and M. R. Swanson. 1973. An evaluation of when genetic selection occurred during the early portion ten pairwise multiple comparison procedures by Monte of the generation in question. If this is true, there is a Carlo methods. J. Am. Stat. Assoc. 68: 66-74. level of ecological unpredictability in the ecology ofB. Dobzhansky, T. 1970. Genetics of the Evolutionary Process. antarctica which is not evident in statistical analyses of Columbia University Press. climatic factors. Downes, J. A. 1965. of insects in the Arctic. Annu. Rev. Entomol. 10: 257-74. Third, because of the limited vagility of adult B. ant- Gressitt, J. L. ed. 1967. Enomology of Antarctica. Vol. 10 arctica, inbreeding may be a significant factor in popu- Antarctic Research Series. NAS-NRC Publication No. lation structure. As a corollary to limited vagility, we 1574. may simply be sampling eggs from a few females. With Kruskal, J. B. 1964. Multidimensional scaling by optimizing our present level of knowledge of the population biology goodness of fit to a nonmetric hypothesis. Psychometrika of B. antarctica, we are unable to accurately evaluate 29: 1-27. the contribution of these factors. Martin, J. 1962. Inversion polymorphism in an Antarctic spe- Fourth, there has been a high level of passive trans- cies living in a simple environment. Am. Nat. 96: 317- 8. port between nearby islands of larval and adult flies both Martin, J., W. Wulker, and J. E. Sublette. 1974. Evolution- by wind and by birds in their nesting materials. As a ary Cytology in the genus Chrionomus Meigen. Stud. Nat. result, the patterns of genetic variation have become Sci. (Eastern N.M. Univ.) 1(12): 1-12. somewhat irrelevant in that the ecological predictors of Morrison, D. F. 1967. Multivariate Statistical Methods. genetic variability no longer apply at this particular time McGraw-Hill Book Co., New York. and place. One must consider that we are dealing with Peckham, V. 1971. Notes on the chironomid midge Belgica individuals collected over ca. a 7-km range in Arthur antarctica. Pac. Insects Monog. 25: 145-66. Harbor, and that considerable levels of passive transport Slobodkin, L. B., and H. L. Sanders. 1969. On the contri- by birds is possible. Passive transport would have 2 an- bution of environmental stability to species diversity. tagonistic affects. It would provide a stochastic compo- Brookhaven Symp. Biology 22: 82-95. nent in the composition of founding colonies as well as Snedecor, G. W. 1956. Statistical Methods. 5th ed. Iowa State Univ. Press. increase gene flow between island populations. Personal Strong, J. 1967. Ecology of terrestrial arthropods at Palmer observation of bird behavior in the Arthur Harbor area Station, Antarctic Pennisula. Antarctic Res. Ser. 10: 357- suggests that passive transport over this small area may 71. be an important facet in explaining part of these results. Torres, B. A. 1953. Sobre la existencia del Tendipedido Bel- While other explanations are possible, we feel that gica antarctica Jacobs en Archipielago Melchion. Mus. some combination of these phenomena have contributed Cuidad Eva Peron, Annl. (N.S.) Buenos Aires. Zool. 1: largely to the observed results. These conclusions about 1-22. adaptive strategies in B. antarctica are obviously highly White, M.J.D. 1973. Animal Cytology and Evolution. Cam- tentative. However, we present them to provide subse- bridge Univ. Press. London. quent investigators with biologically realistic hypotheses Wirth, W. W., and J. L. 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