Heterochrony in the evolution of Trinidadian guppy offspring size: maturation along a uniform ontogenetic trajectory.

The size and maturity of Trinidadian guppy (Poecilia reticulata) offspring vary among populations adapted to environments of differential predation. Guppy offspring born to low-predation, high-competition environments are larger and more mature than their high-predation ancestors. Here we ask: what specific changes in developmental or birth timing occur to produce the larger, more mature neonates? We collected specimens across the perinatal window of development from five populations and quantified musculoskeletal maturation. We found that all populations undergo similar ontogenetic trajectories in skeletal and muscle acquisition; the only difference among populations is when neonates emerge along the trajectory. The smallest neonates are born with 20% of their skeleton ossified, whereas the largest neonates are born with over 70% of their skeleton ossified. The area of the major jaw-closing muscle is relatively larger in larger offspring, scaling with length as L2.5 The size range over which offspring are birthed among populations sits along the steepest part of the size-maturity relationship, which provides a large marginal increase in fitness for the high-competition female. Because of the functional effects of producing more mature offspring at birth, offspring size may be the first and most critical life-history trait selected upon in highly competitive environments.

Morphological and functional maturity of the oral jaws covary with offspring size in Trinidadian guppies.

Large size of individual offspring is routinely selected for in highly competitive environments, such as in low-predation populations of the Trinidadian guppy (Poecilia reticulata). Large guppy offspring outcompete their smaller conspecifics, but the functional mechanisms underlying this advantage are unknown. We measured jaw kinematics during benthic feeding and cranial musculoskeletal morphologies in neonates and juveniles from five populations of Trinidadian guppy and found that both kinematics and morphologies vary substantially with neonatal size. Rotation at the intramandibular joint (IMJ), but not the quadratomandibular joint (QMJ), increases with size among guppy offspring, from 11.7° in the smallest neonates to 22.9° in the largest neonates. Ossification of the cranial skeleton varies from 20% in the smallest neonates to 90% in the largest. Relative to standard length (SL; jaw tip to caudal fin base distance), the surface area of jaw-closing musculature scales with positive allometry (SL2.72) indicating that muscle growth outpaces body growth. Maximum gape also scales with positive allometry (SL1.20), indicating that larger neonates are capable of greater jaw excursions. These findings indicate that size is not the sole adaptive benefit to producing larger offspring; maturation provides a potential functional mechanism underlying the competitive advantage of large offspring size among Trinidadian guppies.