Specialization of male reproductive tactics correspond with large gonads and small brains

Abstract

Sexual selection has strong effects on gonad size, which has been proposed to shift energetic allocations resulting in concomitant decreases to brain size. However, mixed findings leave it unclear whether negative correlations arise from direct energetic trade-offs or correlated selection. We tested whether male reproductive tactics impose energetic trade-offs by comparing brain and gonad sizes in Poecilia parae, a fish with discrete alternative male morphs specializing in three reproductive strategies: coercion, display, and sneaking. The obligate sneaker morph had substantially larger gonads and smaller brains than the other morphs, consistent with an energetic trade-off. However, examining individuals within morphs revealed a positive relationship, contradicting energetic trade-offs. To resolve which morphs reflect the ancestral state, we examined two closely related species whose males utilize more flexible reproductive strategies, Poecilia picta and Poecilia reticulata. Within these species, a negative correlation between gonad and brain size was observed, consistent with correlated selection shaping traits towards multiple reproductive peaks. Additionally, neuron-to-glia ratio (a proxy for energetic demands) showed no link to gonad size. Our results suggest that reproductive strategies shape brain evolution through correlated selection rather than direct energetic trade-offs, challenging assumptions of sexually selected traits imposing constraints through direct resource allocation.