SUMMARYPrecocial development, in which juveniles are relatively mature at hatching or birth, is more common among vertebrates than altricial development, and is likely to be the basal condition. Altricial development characterizes many birds and mammals and is generally viewed as an alternate strategy, promoting fast growth rates, short developmental periods and relatively poor locomotor performance prior to attaining adult size. Many aquatic birds such as Anseriformes (ducks, geese and swans), Charadriformes (gulls and terns) and Gruiformes (rails) undergo distinctive developmental trajectories, in that hatchlings are able to run and swim the day they hatch, yet they do not begin to fly until fully grown. We hypothesized that there should be tradeoffs in apportioning bone and muscle mass to the hindlimb and forelimb that could account for these patterns in locomotor behavior within the mallard (Anas platyrhynchos). Growth of the musculoskeletal system in the forelimbs and hindlimbs was measured and compared with maximal aquatic and terrestrial sprint speeds and aerial descent rates throughout the 2-month-long mallard ontogenetic period. At 30days post hatching, when body mass is 50% of adult values, hindlimb muscle mass averages 90% and forelimb muscle mass averages 10% of adult values; similarly, bone growth (length and width) in the hindlimbs and forelimbs averages 90 and 60% of adult values, respectively. The attainment of mallard locomotor performance parallels the morphological maturation of forelimb and hindlimb morphometrics -hindlimb performance initiates just after hatching at a relatively high level (~50% adult values) and gradually improves throughout the first month of development, while forelimb performance is relatively non-existent at hatching (~10% adult values), experiencing delayed and dramatic improvement in function, and maturing at the time of fledging. This divergence in ontogenetic strategy between locomotor modules could allow developing Anseriformes to inhabit aquatic, predator-reduced refuges without relying on flight for juvenile escape. Furthermore, by freeing the forelimbs from locomotor demand early in ontogeny, Anseriformes may bypass the potential canalization (i.e. retention) of juvenile form present within their precocial hindlimbs, to dramatically depart in forelimb form and function in the adult. Supplementary material available online at
Summary The livebearing Trinidadian guppy (Poecilia reticulata) produces bigger offspring in populations exposed to low predation and produces smaller, more numerous offspring in populations subject to high predation (HP). Like most fishes, guppies respond to predator attacks with a fast‐start escape response. From the scaling of teleost fast‐start performance, we predict that larger guppy neonates should exhibit faster, more effective escape responses than smaller neonates. Increasing performance with increasing size could be due simply to size, or to both size and the acquisition of more mature body forms, as is seen in larval‐stage fishes. We find no difference in external body proportions among guppy offspring varying in size from 5·1 mm to 7·1 mm at birth, suggesting offspring are born morphologically mature. However, based on the degree of skeletal ossification, as a proxy for internal maturity, we find that guppies are still maturing rapidly around the time of birth. The smallest neonates from the very HP Caroni confluence lack ossification of key skeletal elements that are present in their larger low predation counterparts. In guppies from the Aripo/Caroni drainage, we show that neonatal escape performance covaries with responsiveness and increases with size along a gradient of HP offspring, but is lower in the largest low predation offspring. The scaling of escape performance in the HP populations performing maximally (scaling with length as L2·76) exceeds predictions from size alone (scaling exponent of L1·0 indicates performance increases linearly with body size). This suggests that guppy neonates, like rapidly developing larval fishes, vary substantially in morphological maturity among populations. The finding that neonatal guppy offspring covary in both size and maturity at birth means that being smaller also means being less mature, which amplifies the negative escape performance effects of being born small. Despite the negative consequences of being born both small and immature, HP environments select heavily for high fecundity, and thus small offspring size. We find selection favours female life‐history traits over offspring escape performance.
SUMMARYWing morphology correlates with flight performance and ecology among adult birds, yet the impact of wing development on aerodynamic capacity is not well understood. Recent work using chukar partridge (Alectoris chukar), a precocial flier, indicates that peak coefficients of lift and drag (C L and C D ) and lift-to-drag ratio (C L :C D ) increase throughout ontogeny and that these patterns correspond with changes in feather microstructure. To begin to place these results in a comparative context that includes variation in life-history strategy, we used a propeller and force-plate model to study aerodynamic force production across a developmental series of the altricial-flying mallard (Anas platyrhynchos). We observed the same trend in mallards as reported for chukar in that coefficients of vertical (C V ) and horizontal force (C H ) and C V :C H ratio increased with age, and that measures of gross-wing morphology (aspect ratio, camber and porosity) in mallards did not account for intraspecific trends in force production. Rather, feather microstructure (feather unfurling, rachis width, feather asymmetry and barbule overlap) all were positively correlated with peak C V :C H . Throughout ontogeny, mallard primary feathers became stiffer and less transmissive to air at both macroscale (between individual feathers) and microscale (between barbs/barbules/barbicels) levels. Differences between species were manifest primarily as heterochrony of aerodynamic force development. Chukar wings generated measurable aerodynamic forces early (<8days), and improved gradually throughout a 100day ontogenetic period. Mallard wings exhibited delayed aerodynamic force production until just prior to fledging (day 60), and showed dramatic improvement within a condensed 2-week period. These differences in timing may be related to mechanisms of escape used by juveniles, with mallards swimming to safety and chukar flap-running up slopes to take refuge. Future comparative work should test whether the need for early onset of aerodynamic force production in the chukar, compared with delayed, but rapid, change in the mallard wing, leads to a limited repertoire of flight behavior in adult chukar compared with mallards. Supplementary material available online at
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.
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.
What is the functional effect of prolonged development? By controlling for size, we quantify first-feeding performance and hydrodynamics of zebrafish and guppy offspring (5 ± 0.5 mm in length), which differ fivefold in developmental time and twofold in ontogenetic state. By manipulating water viscosity, we control the hydrodynamic regime, measured as Reynolds number. We predicted that if feeding performance were strictly the result of hydrodynamics, and not development, feeding performance would scale with Reynolds number. We find that guppy offspring successfully feed at much greater distances to prey (1.0 vs. 0.2 mm) and with higher capture success (90 vs. 20%) compared with zebrafish larvae, and that feeding performance was not a result of Reynolds number alone. Flow visualization shows that zebrafish larvae produce a bow wave 0.2 mm in length, and that the flow field produced during suction does not extend beyond this bow wave. Due to well-developed oral jaw protrusion, the similar-sized suction field generated by guppy offspring extends beyond the horizon of their bow wave, leading to successful prey capture from greater distances. These findings suggest that prolonged development and increased ontogenetic state provides first-feeding fish time to escape the pervasive hydrodynamic constraints (bow wave) of being small.
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