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Patterns of Gene Flow and Genetic Structure in Cave-Dwelling Crickets of the Tuscan Endemic, Dolichopoda Schiavazzii (Orthoptera, Rhaphidophoridae)

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Patterns of Gene Flow and Genetic Structure in Cave-Dwelling Crickets of the Tuscan Endemic, Dolichopoda Schiavazzii (Orthoptera, Rhaphidophoridae) Heredity 78(1997) 665—673 Received27 September 1996 Patterns of gene flow and genetic structure in cave-dwelling crickets of the Tuscan endemic, Dolichopoda schiavazzii (Orthoptera, Rhaphidophoridae) GIULIANA ALLEGRUCCI*, MARIA GIULIA MINASI & VALERIO SBORDONI Dipartimento di Biologia, Università degli Studi di Roma 'Tor Vergata Via della Ricerca Scientifica, 00133 Rome, Italy Dolichopodaschiavazzii is a cave cricket species endemic to Tuscany, Italy. This species inhabits natural limestone caves and also man-made hypogean environments. Dolichopoda schiavazzii can colonize new environments both passively and actively. This species shows a metapopulational structure depending on both the cave's external bioclimatic conditions and the geographical distance. This paper reports data on 26 allozyme loci in nine populations of D. s. schiavazzii and in one of D. s. caprai, investigates their genetic structuring and provides measures of gene flow between them at different geographical scales. Some loci showed heterozygote deficiencies, probably owing to the Wahlund effect, caused by the mixing of individuals belonging to two different cohorts. Genetic subdivision is high, particularly among populations inhabiting caves located on the Tyrrhenian coast. The mean FST (0 estimator) across populations was 0.34. An analysis of the gene flow levels, carried out by comparing pairwise Nm values, indicates that the number of migrants drops as the geographical distance increases, suggesting the actual occurrence of gene flow only between geographically close populations in an inner area of Tuscany where the occurrence of mesophilous woods might favour migration between caves. The general picture, however, is one of a substantial lack of gene flow, even if a significant trend of isolation by distance is found, probably reflecting historical gene flow. Keywords:allozymes,cave crickets, gene flow, population genetics. individuals are sometimes observed in moist or Introduction mesic woods. Dolichopoda schiavazzii is one of the Overthe past several years, our laboratory has nine species present in Italy; it is endemic to carried out geographical surveys of genetic varia- Tuscany, being distributed throughout the western bility within a number of cave cricket species, part of this region, and the two islands of Elba and belonging to the genus Dolichopoda, distributed Pianosa. In addition to natural limestone caves, throughout peninsular and insular Italy. These several populations inhabit man-made hypogean studies were carried out by combining several meth- environments, such as cellars, catacombs, aqueducts odologies and approaches to elucidate patterns of and Etruscan tombs. Within the species range, some adaptation, population divergence and speciation populations seem to exhibit a metapopulational (Sbordoni et a!., 1985, 1987, 1991; Allegrucci et a!., structure, in which gene flow could occur to some 1992; Venanzetti et a!., 1993). extent between geographically close demes. Unlike Most species of this genus are dependent on other Dolichopoda species, D. schiavazzii is suscep- caves. However, several populations inhabit cave- tible to passive dispersal and capable of colonizing like habitats, such as rock crevices and ravines, and new environments. In a few artificial caves of the Argentario promontory, it coexists with D. baccettii, * Correspondence.E-mail: [email protected] where secondary contact and hybridization pheno- 1997The Genetical Society of Great Britain. 665 666 G. ALLEGRUCCI ETAL. mena have also been reported (Allegrucci et a!., s. caprai was also studied. The population samples 1982). The occurrence of D. schiavazzii in this area represented the distribution range of D. schiavazzii. seems to result from anthropocore dispersal, prob- The object of this paper is to determine the ably dating back to the middle of the eighteenth amount of genetic divergence and levels of gene century, after the foundation of the religious house flow within this discontinuously distributed species. 'Padri Passionisti', located near the caves. Morpho- This is an attempt to assess the genetic structure of logically, D. schiavazzii can be clearly discriminated a species in which the process of adaptation to cave from other Dolichopoda species by its spines on the life and isolation in caves has still not been femurs of the second and third pairs of legs. On this completed. basis, a different subspecies, D. schiavazzii caprai, The allozyme data will also be compared with the has been described with a reduced number of spines satellite DNA sequence data. along the inferior borders of the femurs of the second pair of legs (Lanza, 1957). Materialsand methods A previous study (Sbordoni et a!., 1985) revealed the occurrence of genetic differentiation between InTable 1, the populations studied are reported populations of D. schiavazzii. On the other hand, the with details on their geographical locations, estima- analysis of a species-specific satellite DNA sequence ted population sizes and sampling dates. of a few populations of D. schiavazzii revealed a very Dolichopoda populations were assayed electro- high degree of sequence homogeneity within the phoretically at 26 gene loci, coding for 21 enzymes. species with no single fixed nucleotide substitution Details on technical procedures are the same as in discriminating any populations (Bachman et a!., Allegrucci et al. (1992). 1994). This outcome was unexpected from the early Allele frequencies, Nei's (1978) genetic distance, allozyme analyses that revealed substantial genetic heterozygosities and other genetic parameters were differentiation between populations. calculated using the BIOSIS-1 program of Swofford & In order to obtain additional detailed information Selander (1981). A tree was drawn using the on the population genetic structure of D. schiavazzii, Reynolds et a!. (1983) index and the neighbour- we increased the number of allozyme loci and popu- joining (NJ tree; Saitou & Nei, 1987) method to lations from the island of Elba to coastal and inland highlight genetic relationships between the studied Tuscany. Some populations were the same as those populations. Both distances and the tree were analysed for satellite DNA sequence. Two popula- obtained using the phylogenetic package PHYLIP 3.57 tions from the Argentario promontory, which were (Felsenstein, 1995). Robustness of each node was the result of human introduction (Allegrucci et a!., evaluated by bootstrapping allele frequencies 100 1982), were also included, and one population of D. times, using the program SEQBOOT in PHYLIP 3.57. Table 1Dolichopodaschiavazzii populations: basic and ecological information on the sampled caves Altitude N Sampling Population Locality Name (m) Latitude Longitude average date D.s. caprai Fichino Bagni di Casciana, P1 FIC 242 43.47 10.52 50 05/94 D.s. schiavazzii Cisternino Cisternino aqueduct, LI CIS 45 43.53 10.40 1877 05/94 Tomba del Belagaio Roccastrada, GR BEL 250 43.07 11.15 360 11/92 Necropoli di PopuloniaPopulonia, LI POP 60 42.95 10.50 1500 02/92 11/92 Grotta dei Pipistrelli Montorsaio, GR ORS 250 42.88 11.20 150 04/92 11/92 Cabinovia di Marciana Isola d'Elba, LI MRC 350 42.78 10.17 200 04/94 Pozzetto di S. Feb Isola d'Elba, LI ELB 150 42.77 10.40 — 05/92 Necropoli di Vetulonia Vetulonia, GR VET 120 42.83 10.97 1000 11/92 Buca sopra Cimitero M.te Argentario, GR BSC 520 42.42 11.01 150 03/92 Convento Passionisti M.te Argentario, GR CPS 520 42.40 11.02 800 11/92 The Genetical Society of Great Britain, Heredity, 78, 665—673. GENE FLOW AND GENETIC STRUCTURE IN CAVE CRICKETS 667 The coancestry index of Reynolds et a!., (1983) was hypotheses at a 0.05 'table-wide' level of significance used because it is appropriate for short-term evolu- (Rice, 1989). tion, when the divergence between populations with To investigate whether isolation by distance is a common ancestral population may be regarded as detectable from the data, a correlation between pair- being caused solely by drift. Nei's index was used to wise Nm and geographical distances was performed compare the present data with those from other by using log transformations (Slatkin, 1993). The Dolichopoda species. significance of the resulting regression was tested Wright's measure of the among-population using a Mantel test between the two matrices component of genetic variance, FST(Wright,1951, (Mantel, 1967). 1965), was used to study the population structure of Estimates of gene flow were computed from the D. schiavazzii.Cockerham'scoancestry coefficient coancestry coefficients, assuming an infinite island (0)wasused as an estimator of FST(Cockerham, model at equilibrium, as Nm =(1—0)140(Wright, 1969; Weir & Cockerham, 1984). 1969). A statistical test of the neutrality hypothesis was used to verify neutrality for the set of polymorphic Results loci (Slatkin, 1982). The sequential Bonferroni procedure was employed to control for the prob- Table2 reports allele frequencies for each popula- ability of incorrectly rejecting one or more true null tion for all loci. Sixteen loci were polymorphic Table 2 Allelefrequencies at 26 allozyme loci in one population of Dolichopoda s. caprai (FIC) and nine of D. s. schiavazzii Locus FIC CISBELPOPORSMRCELBVETBSCCPS N* 10 20 10 30 25 40 18 25 10 30 Aat A 0.0000.0000.0000.0810.0000.2430.0280.0000.0000.000 B 1.0001.0001.0000.9191.0000.757 0.9721.0001.0001.000 Acp A 1.0001.0001.0001.0001.0001.0001.0001.0001.0001.000 Ada B 0.8500.9120.6430.3750.8890.0000.3750.1670.5000.750 C 0.1500.0880.3570.2810.1110.8610.6250.7500.500
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