Morphometric analysis of wild-caught flies of Drosophila (Diptera: Drosophilidae) species: Altitudinal pattern of body size traits, wing morphology and sexual dimorphism

Abstract

Literature concerning phenotypic variation among wild-caught drosophilids inhabiting varied ecological habitats is relatively rare. The present study explores pattern of body size traits along altitudinal gradients, and compensation to colder environments and reduced air pressure via adjustment of wing morphology at higher altitudes. Wild adult flies were collected in two extensive surveys during September-October 2014 and April-May 2015. All traits were measured for both the sexes to obtain data on sexual dimorphism. It was found that though these populations differed significantly in their size, as already known, they deviated from the expected reaction norms of size increase along altitudinal gradients as observed in several previous studies. This deviation from normal clinal trend can be attributed to variation in growth rates and development times at different altitudes which has important implications in overall reproductive success. Also, a significant increase in wing area of flies at higher altitude was recorded with dramatically lower wing loadings than flies that developed in comparatively warmer habitats, giving them an aerodynamic advantage at cold temperatures. Thorax width was also analyzed, possibly for the first time in wild-caught flies of Indian populations, revealing sexual dimorphism. The ratio of thorax length to width was greater than one for all species indicating that the thorax is more elongated in females, which may also influence the flight capacity of the sexes.

Keywords

• Bergmann rule,Diptera,Drosophilidae,morphometric traits,plasticity

Doğadan yakalanan Drosophila (Diptera: Drosophilidae) türlerinin morfometrik analizi: Vücut büyüklüğü özelliklerinin yüksekliğe bağlı değişimi, kanat morfolojisi ve eşeysel dimorfizmi

Öz

Çeşitli ekolojik habitatlarda yaşayan doğadan toplanmış Drosophila türleri arasındaki fenotipik çeşitlilik ile ilgili literatür sayısı nispeten azdır. Bu çalışmada vücut boyutu özelliklerinin yükseklik eğrileri boyunca olan uyumu ve daha yüksek yerlerde kanat morfolojisinin değişimiyle daha soğuk ortamlara ve daha düşük hava basıncına uyum sağlanması incelenmiştir. Doğadan ergin sinekler, Eylül-Ekim 2014 ve Nisan-Mayıs 2015 tarihlerinde iki kapsamlı sürvey ile toplanmıştır. Eşeysel dimorfizmi hakkında bilgi edinmek için her iki cinste de tüm özellikler ölçülmüştür. Bilindiği gibi, bu popülasyonların boyutlarında önemli farklılıklar olmasına rağmen, daha önceki birçok çalışmada gözlemlendiği gibi, yükseklik eğrileri boyunca boyut artışının beklenen reaksiyon normlarından sapmış oldukları bulunmuştur. Normal klinal eğimindeki bu sapma, genel üreme başarısında önemli etkileri olan farklı yüksekliklerde büyüme hızlarındaki ve gelişim zamanlarındaki farklılıklara bağlanabilir. Ayrıca, yüksek irtifadaki sineklerin kanat alanlarındaki önemli bir artış, karşılaştırmalı olarak daha sıcak habitatlarda gelişen sineklerden dramatik olarak çok daha düşük kanat yükleri ile rekor kırmış olmaları sayesinde onlara soğuk hava koşullarında aerodinamik bir avantaj sağlamıştır. Bu arada, muhtemelen Hint popülasyonlarının doğadan yakalanmış sineklerinde ilk kez, Thoraks genişliği, cinsel dimorfizmi açığa çıkararak analiz edilmiştir. Thoraks uzunluğunun genişliğe oranı tüm türler için birden fazla olup; bu da eşeylerin uçuş kapasitesini etkileyebilen thoraksın dişilerde daha uzun olduğunu göstermektedir.

Anahtar Kelimeler

• Bergmann kuralı,Diptera,Drosophilidae,morfometrik özellikler,plastisite

References

1. Angilletta, M.J., T.S. Steury & M.W. Sears, 2004. Temperature growth rate and body size in ectotherms: fitting pieces of a life history puzzle. Integrative and Comparative Biology, 44: 498-509.
2. Atkinson, D. & R.M. Sibly, 1997. Why are organisms usually bigger in colder environments? Making sense of a life history puzzle. Trends in Ecology and Evolution, 12: 235-239.
3. Azevedo, R.B.R., A.C. James, J. McCabe & L. Partridge, 1998. Latitudinal variation of wing: thorax size ratio and wing-aspect ratio in Drosophila melanogaster. Evolution, 52: 1353-1362.
4. Bergmann, C., 1847. Uber die Verh Altnisse der WArme Okonomie der Thiere zu ihrer Grosse. Gottinger Studien, 3: 595-708.
5. Capy, P., E. Pla & J.R. David, 1993. Phenotypic and genetic variability of morphometrical traits in natural populations of Drosophila melanogaster and D. simulans I Geographic variations. Genetics Selection Evolution, 25: 517-536.
6. Carreira, V.P., J. Mensch, E. Hasson & J.J. Fanara, 2016. Natural Genetic Variation and Candidate Genes for Morphological Traits in Drosophila melanogaster. PLoS ONE, 11(7): e0160069.
7. Chown, S.L. & K.J. Gaston, 2010. Body size variation in insects: a macro-ecological perspective. Biological Reviews, 85: 139-169.
8. Chown, S.L. & C.J. Klok, 2003. Altitudinal body size clines: latitudinal effects associated with changing seasonality. Ecography, 26: 445-455.

9. Daly, H.V., 1985. Insect morphometrics. Annual Reviews of Entomology, 30: 415-438.
10. David, J.R., L.O. Araripe, B.C. Bitner-Mathe, P. Capy, B. Goni, L.B. Klaczko, H. Legout, M.B. Martins, J. Vouidibio, A. Yassin & B. Moreteau, 2006a. Quantitative trait analysis and geographic variability of natural populations of Zaprionus indianus, a recent invader in Brazil. Heredity, 96: 53-62.
11. David, J.R., P. Gibert, S. Mignon-Grasteau, H. Legout, G. Petavy, C. Beaumont & B. Moreteau, 2003. Genetic variability of sexual sex dimorphism in a natural population of Drosophila melanogaster: an isofemale line approach. Journal of Genetics, 82: 101-110.
12. David, J.R., H. Legout & B. Moreteau, 2006b. Phenotypic plasticity of body size in a temperate population of Drosophila melanogaster: when the temperature-size rule does not apply. Journal of Genetics, 85: 9-23.
13. David, J.R., P. Gibert & B. Moreteau, 2004. “Evolution of reaction norms”. In: Phenotypic plasticity-Functional and conceptual approaches (Eds. T.J. DeWitt and S.M. Scheiner). Oxford University Press, 50-63.
14. David, J.R., P. Gibert, E. Gravot, G. Petavy, J.P. Morin, D. Karan & B. Moreteau, 1997. Phenotypic plasticity and developmental temperature in Drosophila: analysis and significance of reaction norms of morphometrical traits. Journal of Thermal Biology, 22: 441-451.
15. David, J.R. & L. Tsacas, 1981. Cosmopolitan subcosmopolitan and widespread species: different strategies within the Drosophilid family (Diptera). CR Society of Biogeography, 57: 11-26.
16. DeWitt, T.J. & S.M. Scheiner, 2004. Phenotypic plasticity-Functional and conceptual approaches. Oxford University Press, Oxford, UK.
17. Dillon, M., M. Frazier & R. Dudley, 2006. In to thin air-Physiology and evolution of alpine insects. Integrative and Comparative Biology, 46(1): 49-61.
18. Dudley, R., 2000. The biomechanics of insect flight-Form, function, evolution. Princeton University Press, Princeton, USA.
19. Frazier, M.R., J.F. Harrison, S.D. Kirkton & S.P. Roberts, 2008. Cold rearing improves cold-flight performance in Drosophila via changes in wing morphology. Journal of Experimental Biology, 211: 2116-2122.
20. García-Barros, E., 2000. Climaytamaño en mariposas diurnas (Lepidoptera: Papilionidae). Boletín de la Asociación Española de Entomología, 24: 47-64.
21. Gibert, P., P. Capy, A. Imasheva, B. Moreteau, J.P. Morin, G. Petavy & J.R. David, 2004. Comparative analysis of morphological traits among Drosophila melanogaster and D. simulans: genetic variability, clines and phenotypic plasticity. Genetica, 120: 165-179.
22. Gilchrist, G.W. & R.B. Huey, 2004. Plastic and genetic variation in wing loading as a function of temperature within and among parallel clines in Drosophila subobscura. Integrative and Comparative Biology, 44: 461-470.
23. Gillooly, J.F., E.L. Charnov, G.B. West, V.M. Savage & J.H. Brown, 2002. Effects of size and temperature on developmental time. Nature, 417: 70-73.
24. Gupta, J.P., 2005. A monograph on Indian Drosophilidae. Journal of Scientific Research, 5: 1-252.
25. Hu, Y.G. & M.J. Toda, 2001. Polyphyly of Lordiphosa and its relationships in Drosophilinae (Diptera: Drosophilidae). Systematic Entomology, 26: 15-31.
26. Huey, R.B., B. Moreteau, J.C. Moreteau, P. Gibert, G.W. Gilchrist, A.R. Ives, T. Garland Jr & J.R. David, 2006 Sexual size dimorphism in a Drosophila clade, the D. obscura group. Zoology, 109: 318-330.
27. Imasheva, A.G., B. Moreteau & J.R. David, 2000. Growth temperature and genetic variability of wing dimensions in Drosophila: opposite trends in two sibling species. Genetics Research, 76: 237-247.
28. James, A.C., R.B.R. Azevedo & L. Partridge, 1997. Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics, 146: 881-890.
29. Karan, D., S. Dubey, B. Moreteau, R. Parkash & J.R. David, 2000. Geographical clines for quantitative traits in natural populations of a tropical drosophilid: Zaprionus indianus. Genetica, 108: 91-100.
30. Karan, D., A.K. Munjal, P. Gibert, B. Moreteau, R. Parkash and J.R. David, 1998. Latitudinal clines for morphometrical traits in Drosophila kikkawai: a study of natural populations from the Indian subcontinent. Genetics Research, 71: 31-38.
31. Klepsatel, P., M. Gáliková, C.D. Huber & T. Flatt, 2014. Similarities and differences in altitudinal versus latitudinal variation for morphological traits in Drosophila melanogaster. Evolution, 68(5): 1385-98.
32. Kumar, R. & K. Ajai, 2009. Studies on Drosophilidae (Diptera: Drosophilidae) of Gujarat state in India. Drosophila Information Services, 92: 106.
33. Loeschke, V., J. Bundgaard & J.S.F. Barker, 2000. Variation in body size and life history traits in Drosophila aldrichi and D. buzzatii from a latitudinal cline in eastern Australia. Heredity, 85: 423-433.
34. Markow, T. & P.M. O’Grady, 2006. Drosophila-A Guide to Species Identification and Use. London Academic Press, London, UK.
35. McAlpine, J.F., 1981. “Morphology and terminology-Adults”. In: Manual of Nearctic Diptera, Agriculture Canada Monograph No. 27 (Eds. J.F. McAlpine et al.). Ontario Biosystematics Research Institute, Ottawa, 1: 9-63.
36. Mousseau, T.A., 1997. Ectotherms follow the converse to Bergmann’s rule. Evolution, 51: 630-632.
37. Norry, F., O. Bubliy & V. Loeschcke, 2001. Developmental time, body size and wing loading in Drosophila buzzatii from lowland and highland populations in Argentina. Hereditas, 135(1): 35-40.
38. Pitchers, W., J.E. Pool & I. Dworkin, 2013. Altitudinal Clinal Variation in Wing Size & Shape in African Drosophila melanogaster: One Cline or Many? Evolution, 67(2): 438-452.
39. Powell, J.R., 1997. Progress and prospects in evolutionary biology- The Drosophila model. Oxford University Press, Oxford, UK.
40. Prevosti, A., 1955. “Geographical variability in quantitative traits in populations of Drosophila subobscura”. Cold Spring Harbor Symposium Quantitative Biology, 20: 294-299.
41. Ray, C., 1960. The application of Bergmann’s and Allen’s rules to poikilotherms. Journal of Morphology, 106: 85-108.
42. Sarswat, M., R.S. Fartyal, P.C. Sati, M. Kandpal & B.K. Singh, 2015. Diversity and distribution pattern of drosophilids (Diptera, Drosophilidae) along an altitudinal transect in Uttarakhand and its implication in cytogenetics & molecular systematics study. Journal of Entomological Research, 39(4): 311-322.
43. Singh, B.N., 2015. Species and genetic diversity in the genus Drosophila inhabiting the Indian subcontinent. Journal of Genetics, 94: 351-361.
44. Smith, R.J., A. Hines, S. Richmond, M. Merrick, A. Drew & R. Fargo, 2000. Altitudinal variation in body size and population density of Nicrophorus investigator (Coleoptera: Silphidae). Environmental Entomology, 29: 290-298.
45. Slatkin, M., 1984. Ecological causes of sexual dimorphism. Evolution, 38: 622-630.
46. Stalker, H.D. (1980) Chromosome studies in wild populations of Drosophila melanogaster. II. Relationship of inversion frequencies to latitude, season, wing-loading and flight activity. Genetics, 95: 211-223.
47. Stalker, H.D. & H.L. Carson, 1947. Morphological variation in natural populations of Drosophila robusta Sturtevant. Evolution, 1: 237-248.
48. Van Voorhies, W.A., 1997. On the adaptive nature of Bergmann size clines: a reply to Mousseau, Partridge and Coyne. Evolution, 51: 635-640.
49. Van’t Land, J., B.J. Zwaan, W.F. Van Putten, A. Kamping & W. Van Delden (1999) Latitudinal variation in wild populations of Drosophila melanogaster: heritabilities and reaction norms. Journal of Evolutionary Biology, 12: 222-232.
50. Zhang, W. & M.J., 1992. A new species-subgroup of the Drosophila immigrans species-group (Diptera, Drosophilidae), with description of two new species from China and revision of taxonomic terminology. Japanese Journal of Entomology, 60: 839-850.