Male-mediated early maturation unlikely to evolve via adaptive evolution

• Published in: Animal behaviour Vol. 214; pp. 219 - 240
• Main Authors: Lerch, Brian A., Zipple, Matthew N., Gesquiere, Laurence R., Sloan, Evan T., Beehner, Jacinta C., Alberts, Susan C.
• Format: Journal Article
• Language: English
• Published: Elsevier Ltd 01.08.2024
• Subjects: Bruce effect; feticide; infanticide; oestrogen; reproductive timing; spandrel; Vandenbergh effect; oestrogen; infanticide; Bruce effect; reproductive timing; spandrel; Vandenbergh effect; feticide
• ISSN: 0003-3472; 1095-8282
• DOI: 10.1016/j.anbehav.2024.06.002

The Vandenbergh effect, or male-mediated maturation, occurs when females reach sexual maturation upon exposure to a novel male. Male-mediated maturation is found across mammals, including in geladas, Theropithecus gelada, where it may be an adaptive counterstrategy to infanticide that follows the immigration of a new male; maturing after male immigration maximizes a female's chances of weaning her first offspring before the next infanticidal male immigrates (the ‘optimal timing hypothesis’). Alternatively, the nonadaptive ‘Bruce effect by-product hypothesis’ posits that male-mediated maturation in geladas (and possibly other mammals) is triggered by the same physiological changes that, in pregnant females, produce spontaneous abortion (the Bruce effect). We test both hypotheses using theory and observational data. We show that neither male-mediated maturation nor its associated hormonal changes occur in baboons (Papio cynocephalus×Papio anubis), a primate without the Bruce effect. An individual-based model suggests that male-mediated maturation should not evolve via adaptive evolution in either geladas or baboons. Finally, we derive the selection coefficient for male-mediated maturation and show it is likely to be very small because male-mediated maturation yields only marginal potential benefits unless the system is extremely fine-tuned. We conclude that male-mediated maturation in geladas is a by-product of the Bruce effect and more broadly that the Vandenbergh effect may be nonadaptive. •Male-mediated maturation does not occur in Amboseli baboons (Papio cynocephalus×Papio anubis).•Female Amboseli baboons do not show an endocrinological response to male immigration.•Male-mediated maturation does not evolve in simulations of two primate populations.•Selection for male-mediated maturation is very weak without extreme fine-tuning.•The Vandenbergh effect may be a by-product of the Bruce effect.