Linking behavioral ecology with population genetics: insights from Drosophila nigrospiracula

摘要

Species of the genus Drosophila exhibit a wide range of differences in the levels of population genetic differentiation observed using allozyme electrophoresis and molecular genetic studies (Powell 1997; Shoemaker and Jaenike 1997; Markow et al. 2002; Hurtado et al. 2004). An absence of relevant behavioral and ecological studies of the majority of these species makes it difficult to interpret the factors responsible for the presence or absence of population structure. Four species of cactophilic Drosophila endemic to the Sonoran Desert of North America, however, have been well characterized with respect to their ecology (Heed 1978, 1982; Breitmeyer and Markow 1998) and behavior (Markow 1982, 1988; Markow and Castrezana 2000). All four species have specialized on different columnar cactus host species, feeding and breeding in necrotic plant tissue or in soil soaked with the necrotic exudates (Heed 1978, 1982). The four Drosophila species show contrasting patterns of population subdivision, permitting hypotheses to be tested concerning the relationship between ecology and behavior and population genetic differentiation.One of the cactophilic species, D. nigrospiracula Patterson & Wheeler, exhibits no population structure across its range, compared to the other three desert endemic species, all of which exhibit some degree of local genetic differentiation. These patterns have been found whether the loci used were allozymes (Sluss 1975; Pfeiler and Markow 2001; Markow et al. 2002) or molecular genetic markers (Hurtado et al. 2004), and for D. nigrospiracula, gene frequencies have been found to be stable for over 30 years (Sluss 1975; Pfeiler and Markow 2001).Potential explanations for the observed lack of population structure and the temporal stability of gene frequencies lie in the behavioral ecology of D. nigrospiracula. Field studies demonstrate that compared to the other desert Drosophila, D. nigrospiracula is a strong disperser (Johnston and Heed 1976; Markow and Castrezana 2000). In the laboratory, flies of D. nigrospiracula have been found to become sexually mature later than those of D. melanogaster: females mate at four and males at six days of age (Markow 1982). Reproductive behavior has been found to differ in other Drosophila species, however, when field and laboratory studies have been compared (Markow 1988, 2000; Snook and Markow 2001). Therefore, while it may be tempting to speculate that long distance dispersal coupled with late reproductive maturity could explain the apparent extensive gene flow in D. nigrospiracula, caution must be exercised in the absence of information about when flies in nature mate relative to when they disperse and oviposit. For example, if D. nigrospiracula mate and oviposit prior to dispersing, adult flies emerging from a given breeding patch would exhibit some degree of inbreeding, as observed in the Opuntia-breeding D. buzzatii (Barker and Mulley 1976). On the other hand, if flies disperse before they mate, not only should local inbreeding be insignificant, but it would promote a lack of population structure. These different scenarios can be distinguished by field studies.Here we ask two questions about D. nigrospiracula: 1) when do flies mate relative to when they disperse? 2) is there evidence of inbreeding at a given micro-habitat patch? We address these questions through capture-mark-release-recapture studies using virgin flies of different ages and with allozyme electrophoresis of resident adults and newly emerged flies at the same patch.