Effects of neonatal size on maturity and escape performance in the Trinidadian guppy

Abstract

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.

Maternal predator‐exposure affects offspring size at birth but not telomere length in a live‐bearing fish

“…First, females responded to predator models and to the alarm cue by showing the typical antipredator behavior observed in natural conditions and as found in previous laboratory experiments (Evans et al, 2007;Heathcote et al, 2017). Second, we found a significant reduction of offspring size at birth, which suggests that the stress experienced by the mothers during the gestation negatively impacted offspring as a reduced size constrains escape performance (Dial et al, 2016;Wolcott, Ojanguren, & Barbosa, 2017) and survival (Henrich, 1988) in fishes. Our result aligns with previous evidence in fishes in which the exposure to glucocorticoids (such as the cortisol) in the mother, and in turn in their eggs (Hwang, Wu, Lin, & Wu, 1992), was followed by the production of smaller offspring compared with offspring produced by undisturbed mothers (Eriksen et al, 2006;McCormick, 1998).…”

“…A prolonged period of heightened oxidative stress is known to impair cellular and organismal functions (Guachalla & Rudolph, 2010) and negatively impact fitness of individuals in the long-term (Slos & Stoks, 2008). For instance, previous studies have shown that early presence of glucocorticoids in the eggs negatively affects offspring size at birth (Eriksen, Bakken, Espmark, Braastad, & Salte, 2006;McCormick, 1998), with potential detrimental effects for survival (Dial, Reznick, & Brainerd, 2016).…”

The effects of familiarity on escape responses in the Trinidadian guppy (Poecilia reticulata)

“…Our results showed that size had a far greater effect in the magnitude of the response 314 than familiarity. This result is consistent with previous studies that have shown that the 315 magnitude of the fast-start response in young fish increases with body length (Dial et al 2015). …”

Maternal size and body condition predict the amount of post‐fertilization maternal provisioning in matrotrophic fish

“…Larger offspring, for instance, perform better when food is scarce and competition for food is high, though the advantage of being relatively larger disappears when competition is insignificant (Bashey, 2008;Leips et al, 2013;Parker & Begon, 1986). In fish, larger offspring have better escape performance (Dial, Reznick, Brainerd, & Marshall, 2016;Gibb, Swanson, Wesp, Landels, & Liu, 2006), which is likely to increase survival in high predation environments. Similarly, larger offspring are more resistant to starvation (Gliwicz & Guisande, 1992), probably because larger offspring contain more maternal reserves that prevent them from starvation under adverse food conditions (Tessier, Henry, Goulden, & Durand, 1983).…”