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The sex-ratio ‘SR’ X-linked meiotic drive system in stalk-eyed flies destroys all Y-bearing sperm. Unlike other SR systems, drive males do not suffer fertility loss. They have greatly enlarged testes, which compensate for gamete killing. We predicted that enlarged testes arise from extended development with resources re-allocated from the accessory glands, as these tend to be smaller in drive males. To test this, we tracked the growth of the testes and accessory glands of wildtype and drive males over 5–6 weeks post-eclosion before males attained sexual maturity. Neither of the original predictions are supported by this data. Instead, we found that the drive-male testes were enlarged at eclosion, reflecting a greater allocation of resources to the testes during pupation. In addition, there was no evidence that the greater allocation of resources to the testes during adult development retarded accessory gland growth. There was evidence of a general trade-off with eyespan, as males with larger relative eyespan had larger accessory glands but smaller testes. These findings support the idea that enlarged testes in drive males arise as an adaptive allocation of resources to traits that enhance male reproductive success.One sentence summaryAdaptive testes enlargement in early development ensures maintenance of fertility in stalk-eyed flies that lose half of their sperm due to meiotic drive