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

Abstract

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.

Spatio‐temporal dynamics of density‐dependent dispersal during a population colonisation

“…Moreover, jaw development can constrain diet and limit the competitive performance of newborn fish (Dial et al . ). Second, juveniles may be susceptible to cannibalistic behaviour by adults (Loekle et al .…”

“…Gut content analyses show that smaller (and therefore younger) guppies consume more invertebrates and algae, and less detritus compared to larger ones (Zandon a et al 2011(Zandon a et al , 2015. Moreover, jaw development can constrain diet and limit the competitive performance of newborn fish (Dial et al 2017). Second, juveniles may be susceptible to cannibalistic behaviour by adults (Loekle et al 1982;Magurran & Seghers 1990;Magurran 2005), which can become important in resource-limited, crowded environments.…”

Longer development provides first‐feeding fish time to escape hydrodynamic constraints

“…Adult poeciliids are specialized for jaw protrusion, an adaptation thought to be particularly useful during substrate feeding (Hernandez, Ferry-Graham, & Gibb, 2008). Even among first-feeding guppy offspring, jaw protrusion is associated with increased feeding capacity (Dial, Hernandez, & Brainerd, 2017). First-feeding guppy offspring also use jaw protrusion during their suction strikes (Figure 6e), and such kinematics distinguish the feeding mechanics of first-feeding guppies and zebrafish.…”

“…The jaw protrusion mechanism has been shown to increase throughout ontogeny in both guppies (Dial, Hernandez, & Brainerd, 2017) and zebrafish (Staab & Hernandez, 2010). It has been shown that guppy offspring are born with the ability to protrude their jaws, and that this ability increases throughout early ontogeny (Dial, Hernandez, & Brainerd, 2017).…”

“…Due to their similarly small size, the offspring of these two species are each predicted to feed at Reynolds numbers in the viscous regime, but what effect on feeding performance has the fivefold difference in developmental time? (Scale bars = 1 mm) [Color figure can be viewed at wileyonlinelibrary.com] Hernandez, & Brainerd, 2017;Dial, Reznick, & Brainerd, 2017). The goals of this study are (a) to identify if these two fish species experience poor feeding performance at first-feeding; (b) identify morphological, kinematic or hydrodynamic traits that correlate with feeding performance; and (c) to understand what effect, if any, the fivefold difference in developmental time has on suction feeding performance at small size.…”