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Migration rate and genetic diversity of two Drosophila maculifrons (Duda, 1927) populations from Highland Araucaria Forest Fragments in Southern Brazil

Flies from the Drosophilidae family have been suggested as appropriated for the assessment of the effects of habitat fragmentation (e.g., Mata et al., 2010MATA, RA., MCGEOCH, M. and TIDON, R., 2010. Drosophilids (Insecta, Diptera) as Tools for Conservation Biology. Natureza & Conservação, vol. 8, no. 1, p. 60-65. http://dx.doi.org/10.4322/natcon.00801009.
http://dx.doi.org/10.4322/natcon.0080100...
). Cavasini et al. (2014)CAVASINI, R., BUSCHINI, MLT., MACHADO, LPB. and MATEUS, RP., 2014. Comparison of Drosophilidae (Diptera) assemblages from two highland Araucaria Forest fragments, with and without environmental conservation policies. Brazilian Journal of Biology, vol. 74, no. 4. evaluated the Drosophilidae assemblages of Araucaria Forest fragments in Guarapuava/PR (southern of Brazil), including one studied here. They concluded that the areas are in intermediate state of conservation, and the size of the preserved area and/or connection with other fragments are important and should be considered for the establishment of conservation units. In this context, we analyzed the genetic variability of D. maculifrons (Duda, 1927), a forest dwelling species that belongs to the guaramunu group, collected in two conservation units of highland Araucaria Forest fragments in Guarapuava/PR, in order to establish parameters of genetic diversity and levels of gene flow. Thus, we expect to obtain insights about the connectivity level and its importance to conservation.

The two areas (Parque Municipal das Araucárias – PMA: 25° 23’ 36” S, 51° 27’ 19” W, with 43 ha; Parque Municipal São Francisco da Esperança – SSF: 25° 03’ 52” S, 51° 17’ 37” W, with 84,7 ha) are located 36 kilometers apart from each other and at about 1,100 m above the sea level. The genetic variability was analyzed using nine allozymatic (Est, Gpdh, Idh, Me, Pgm, Hk, Mdh-1, Mdh-2 and Mdh-3Mateus and Sene, 2003Mateus, RP. and Sene, FM., 2003. Temporal and spatial allozyme variation in the South American cactophilic Drosophila antonietae (Diptera; Drosophilidae). Biochemical Genetics, vol. 41, no. 7-8, p. 219-233. http://dx.doi.org/10.1023/A:1025506301239. PMid:14587665
http://dx.doi.org/10.1023/A:102550630123...
) and nine microsatellite loci (034, 053, 057, 087, 095, 096, 099, 102 and 118 – Laborda et al., 2009LABORDA, PR., KLACZKO, LB. and SOUZA, AP., 2009. Drosophila mediopunctata microsatellites. II: Cross- species amplification in the tripunctata group and other species. DrosophilaConservation Genetics Resources, vol. 1, no. 1, p. 281-296. http://dx.doi.org/10.1007/s12686-009-9069-9.
http://dx.doi.org/10.1007/s12686-009-906...
). For allozyme data, the parameter Θ and migration rates M were inferred through the MIGRATE-n v3.6.4 software (Beerli, 2012BEERLI, P., 2012. MIGRATE documentation (version 3.2.1). Technical Report. Available from: <http://popgen.sc.fsu.edu>. Access in: 28 Apr. 2014.). Assuming an average mutation rate of 1.28x10–6 per locus per generation (Voelker et al., 1980Voelker, RA., Schaffer, HE. and Mukai, T., 1980. Spontaneous allozyme mutations in : rate of occurrence and nature of the mutants. Drosophila melanogasterGenetics, vol. 94, no. 4, p. 961-968. PMid:17249027.), average Θ estimates were translated to estimates of average effective population sizes (i.e. Ne = Θ/4μ) for each population.

The allozymatic genetic diversities (Ho) for both populations (Table 1) were lower than those found by Saavedra et al. (1995)SAAVEDRA, CCR., VALENTE, VLS. and NAPP, M., 1995. An ecological/genetic approach to the study of enzymatic polymorphisms in Drosophila maculifrons.Brazilian Journal of Genetics, vol. 18, no. 2, p. 147-164. for D. maculifrons (0.2831) in the Rio Grande do Sul state, Brazil. They were also lower than those found by Machado et al. (2012)MACHADO, LPB., SILVA, DC., SIMÃO, DP. and MATEUS, RP. 2012. Spatial variation of genetic diversity in Drosophila species from two different South America environments. In CALISKAN, M. Genetic variation in animals. Rijeka: Intech. p. 45-62.. http://dx.doi.org/10.5772/32971.
http://dx.doi.org/10.5772/32971...
for D. ornatifrons (Duda, 1927), a closely related species of D. maculifrons, collected in the same areas (PMA – 0.3609; SSF – 0.4060). It is noteworthy that, for allozymes, D. maculifrons and D. ornatifrons of SSF showed higher genetic diversity. For microsatellites, the Ho values obtained (Table 1) were lower than those found by Heinz (2012)HEINZ, NP., 2012. Variabilidade molecular sazonal de Drosophila mediopunctata (Diptera: Drosophilidae). Guarapuava: UNICENTRO. Dissertação de Mestrado. for D. mediopunctata (Dobzhansky and Pavan, 1943), a closely related species of the tripunctata group, in two areas of Guarapuava/PR, PMA (0.5385) and Fazenda Brandalise (0.5062).

Table 1
Allozymes and microsatellites genetic variability parameters for two Drosophila maculifrons natural populations from Guarapuava/PR (Brazil).

For allozymes, the genetic distance indexes resulted in a low to moderate differentiation between PMA and SSF (Nei’s D = 0.0248; Fst = 0.0556). Low genetic differentiation for D. maculifrons was also recently detected for COI and COII mitochondrial genes (Cenzi de Ré et al., 2014CENZI DE RÉ, FC., GUSTANI, EC., OLIVEIRA, APF., MACHADO, LPB., MATEUS, RP., LORETO, ELS. and ROBE, LJ., 2014. Brazilian populations of . Drosophila maculifrons (Diptera, Drosophilidae): low diversity levels and signals of a population expansion after the Last Glacial MaximumBiological Journal of the Linnean Society. Linnean Society of London, vol. 112, no. 1, p. 55-66. http://dx.doi.org/10.1111/bij.12244.
http://dx.doi.org/10.1111/bij.12244...
). On the other hand, for microsatellites, low genetic differentiation was not observed (D = 0.4174; Fst = 0.0901), probably because of its high variability. Therefore, despite the two populations are somewhat genetically similar (see Table 1), they depict some degree of differentiation. This is corroborated by PMA showing one locus less than SSF for both markers, and both populations presented several exclusive alleles (PMA: allozymes - 5; microsatellites - 13; SSF: allozymes - 3; microsatellites - 33).

The migration rates and population size estimations showed that SSF supplies much more migrants to PMA than otherwise (MSSF→PMA = 2,160; MPMA→SSF = 12.416), contributing to a higher average effective population size to PMA (NePMA = 4.629 x 1016; NeSSF = 8.496 x 103). Theses results indicated that size (of the fragment) matters regarding migration. SSF is a conservation unit twice larger than PMA (not taking in account that SSF is surrounded by several other fragments of Araucaria forest in private properties, which must double or even triple the total size of the area, and PMA is surrounded by crop plantations and Guarapuava city limits) and this is probably driving the high rates of migrants between these areas (e.g., Schiffer et al., 2007Schiffer, M., Kennington, WJ., Hoffmann, AA. and Blacket, MJ., 2007. Lack of genetic structure among ecologically adapted populations of an Australian rainforest Drosophila species as indicated by microsatellite markers and mitochondrial DNA sequences. Molecular Ecology, vol. 16, no. 8, p. 1687-1700. http://dx.doi.org/10.1111/j.1365-294X.2006.03200.x. PMid:17402983
http://dx.doi.org/10.1111/j.1365-294X.20...
). Moreover, the amount of migration detected is probably the main cause of the low genetic differentiation found for allozymes here, but other evolutionary forces, such as genetic drift and mutation rates, for example, must be in action to generate and maintain the differentiation detected for microsatellites.

Acknowledgements

Funds were provided by CNPq (RP Mateus, grant number 479719/2011-0), SETI/Fundação Araucária (R. P. Mateus, grant number 868/2012); CAPES (DC Silva Master’s Fellowship); FINEP; and UNICENTRO.

References

  • BEERLI, P., 2012. MIGRATE documentation (version 3.2.1). Technical Report. Available from: <http://popgen.sc.fsu.edu>. Access in: 28 Apr. 2014.
  • CAVASINI, R., BUSCHINI, MLT., MACHADO, LPB. and MATEUS, RP., 2014. Comparison of Drosophilidae (Diptera) assemblages from two highland Araucaria Forest fragments, with and without environmental conservation policies. Brazilian Journal of Biology, vol. 74, no. 4.
  • CENZI DE RÉ, FC., GUSTANI, EC., OLIVEIRA, APF., MACHADO, LPB., MATEUS, RP., LORETO, ELS. and ROBE, LJ., 2014. Brazilian populations of . Drosophila maculifrons (Diptera, Drosophilidae): low diversity levels and signals of a population expansion after the Last Glacial MaximumBiological Journal of the Linnean Society. Linnean Society of London, vol. 112, no. 1, p. 55-66. http://dx.doi.org/10.1111/bij.12244.
    » http://dx.doi.org/10.1111/bij.12244
  • HEINZ, NP., 2012. Variabilidade molecular sazonal de Drosophila mediopunctata (Diptera: Drosophilidae). Guarapuava: UNICENTRO. Dissertação de Mestrado.
  • LABORDA, PR., KLACZKO, LB. and SOUZA, AP., 2009. Drosophila mediopunctata microsatellites. II: Cross- species amplification in the tripunctata group and other species. DrosophilaConservation Genetics Resources, vol. 1, no. 1, p. 281-296. http://dx.doi.org/10.1007/s12686-009-9069-9.
    » http://dx.doi.org/10.1007/s12686-009-9069-9
  • MACHADO, LPB., SILVA, DC., SIMÃO, DP. and MATEUS, RP. 2012. Spatial variation of genetic diversity in Drosophila species from two different South America environments. In CALISKAN, M. Genetic variation in animals. Rijeka: Intech. p. 45-62.. http://dx.doi.org/10.5772/32971.
    » http://dx.doi.org/10.5772/32971
  • MATA, RA., MCGEOCH, M. and TIDON, R., 2010. Drosophilids (Insecta, Diptera) as Tools for Conservation Biology. Natureza & Conservação, vol. 8, no. 1, p. 60-65. http://dx.doi.org/10.4322/natcon.00801009.
    » http://dx.doi.org/10.4322/natcon.00801009
  • Mateus, RP. and Sene, FM., 2003. Temporal and spatial allozyme variation in the South American cactophilic Drosophila antonietae (Diptera; Drosophilidae). Biochemical Genetics, vol. 41, no. 7-8, p. 219-233. http://dx.doi.org/10.1023/A:1025506301239. PMid:14587665
    » http://dx.doi.org/10.1023/A:1025506301239
  • SAAVEDRA, CCR., VALENTE, VLS. and NAPP, M., 1995. An ecological/genetic approach to the study of enzymatic polymorphisms in Drosophila maculifrons.Brazilian Journal of Genetics, vol. 18, no. 2, p. 147-164.
  • Schiffer, M., Kennington, WJ., Hoffmann, AA. and Blacket, MJ., 2007. Lack of genetic structure among ecologically adapted populations of an Australian rainforest Drosophila species as indicated by microsatellite markers and mitochondrial DNA sequences. Molecular Ecology, vol. 16, no. 8, p. 1687-1700. http://dx.doi.org/10.1111/j.1365-294X.2006.03200.x. PMid:17402983
    » http://dx.doi.org/10.1111/j.1365-294X.2006.03200.x
  • Voelker, RA., Schaffer, HE. and Mukai, T., 1980. Spontaneous allozyme mutations in : rate of occurrence and nature of the mutants. Drosophila melanogasterGenetics, vol. 94, no. 4, p. 961-968. PMid:17249027.

Publication Dates

  • Publication in this collection
    Jan-Mar 2015

History

  • Received
    26 May 2014
  • Accepted
    30 June 2014
Instituto Internacional de Ecologia R. Bento Carlos, 750, 13560-660 São Carlos SP - Brasil, Tel. e Fax: (55 16) 3362-5400 - São Carlos - SP - Brazil
E-mail: bjb@bjb.com.br