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Bactrocera tryoni is a polyphagous fruit fly that is predicated to have continuous breeding in tropical and subtropical Australia as temperature and hosts are not limiting. Nevertheless, in both rainforest and tropical agricultural systems, the fly shows a distinct seasonal phenology pattern with an autumn decline and a spring emergence. Temperature based population models have limited predictive capacity for this species and so the driver(s) for the observed phenology patterns are unknown. Using a demographic approach, we studied the age-structure of B. tryoni populations in subtropical Australia in an agricultural system, with a focus on times of the year when marked changes in population abundance occur. We found that the age-structure of the population varied with season: summer and autumn populations were composed of mixed-age flies, while late-winter and early-spring populations were composed of old to very old individuals. When held at a constant temperature, the longevity of adult reference cohorts (obtained from field infested fruits) also showed strong seasonality; the adults of spring and early autumn populations were short-lived, while late autumn and late winter adults were long-lived. While still expressing in modified landscapes, the data strongly suggests that B. tryoni has an endogenous mechanism which would have allowed it to cope with changes in the breeding resources available in its endemic monsoonal rainforest habitat, when fruits would have been abundant in the late spring and summer (wet season), and rare or absent during late autumn and winter (dry season). [ABSTRACT FROM AUTHOR]