Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Rollinson, Njal; Hutchings, Jeffrey A.

doi:10.1007/s00442-011-1945-9

Cited by 26 publications

(25 citation statements)

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“…Egg size has been found to have a large effect on early growth and survival of salmonids [59], [60] and it is possible that the large individual differences revealed by our analysis might be related to variation in egg size (maternal effect; [61]) in addition to differences in early rearing [62]. In addition, we found significant differences in the freshwater growth of sea trout inhabiting two neighbouring rivers.…”

Section: Discussionmentioning

confidence: 61%

“…In addition, we found significant differences in the freshwater growth of sea trout inhabiting two neighbouring rivers. This serves to highlight the large influence that, in addition to maternal effects [62], local-scale rearing conditions may have on juvenile salmonids during early life [53], [63]. The significant effect of body size in our model further suggests the growth experienced in freshwater has a positive effect on length at maturity.…”

Section: Discussionmentioning

confidence: 72%

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Mixed-Effects Modelling of Scale Growth Profiles Predicts the Occurrence of Early and Late Fish Migrants

et al. 2013

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Fish growth is commonly used as a proxy for fitness but this is only valid if individual growth variation can be interpreted in relation to conspecifics' performance. Unfortunately, assessing individual variation in growth rates is problematic under natural conditions because subjects typically need to be marked, repeated measurements of body size are difficult to obtain in the field, and recaptures may be limited to a few time events which will generally vary among individuals. The analysis of consecutive growth rings (circuli) found on scales and other hard structures offers an alternative to mark and recapture for examining individual growth variation in fish and other aquatic vertebrates where growth rings can be visualized, but accounting for autocorrelations and seasonal growth stanzas has proved challenging. Here we show how mixed-effects modelling of scale growth increments (inter-circuli spacing) can be used to reconstruct the growth trajectories of sea trout (Salmo trutta) and correctly classify 89% of individuals into early or late seaward migrants (smolts). Early migrants grew faster than late migrants during their first year of life in freshwater in two natural populations, suggesting that migration into the sea was triggered by ontogenetic (intrinsic) drivers, rather than by competition with conspecifics. Our study highlights the profound effects that early growth can have on age at migration of a paradigmatic fish migrant and illustrates how the analysis of inter-circuli spacing can be used to reconstruct the detailed growth of individuals when these cannot be marked or are only caught once.

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Section: Discussionmentioning

confidence: 61%

Section: Discussionmentioning

confidence: 72%

Mixed-Effects Modelling of Scale Growth Profiles Predicts the Occurrence of Early and Late Fish Migrants

et al. 2013

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“…But despite these observations, direct experimental manipulation has yet to provide clear support for any sibling interaction hypothesis (Einum & Fleming, 1999; Table 2 in Tamate & Maekawa (2000)]. Lalonde, 2005;Takahashi, Makino & Sakai, 2005;Plaistow, Lapsley & Benton, 2006;Plaistow et al, 2007;Rollinson & Hutchings, 2010;Eberhart & Tielbörger, 2012), or hypotheses invoking maternal influences on w(I ) that are independent of sibling interactions (Rollinson & Hutchings, 2011;Louhi et al, 2015). ), each data point is a unique species [redrawn from Closs et al (2013)].…”

Section: Maternal Size Affects the Relationship Between I And Offmentioning

confidence: 99%

“…This is because an association between variation in w(I ) and maternal body size is unlikely in many species, and in fact, even when these associations are likely, direct evidence fails to support the hypothesis (Takahashi et al, 2005;Acolas et al, 2008;Rollinson & Hutchings, 2011;Louhi et al, 2015). This is because an association between variation in w(I ) and maternal body size is unlikely in many species, and in fact, even when these associations are likely, direct evidence fails to support the hypothesis (Takahashi et al, 2005;Acolas et al, 2008;Rollinson & Hutchings, 2011;Louhi et al, 2015).…”

Section: (2) Avenues Of Future Inquirymentioning

confidence: 99%

The positive correlation between maternal size and offspring size: fitting pieces of a life‐history puzzle

Rollinson

Rowe

2015

Biological Reviews

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The evolution of investment per offspring (I) is often viewed through the lens of the classic theory, in which variation among individuals in a population is not expected. A substantial departure from this prediction arises in the form of correlations between maternal body size and I, which are observed within populations in virtually all taxonomic groups. Based on the generality of this observation, we suggest it is caused by a common underlying mechanism. We pursue a unifying explanation for this pattern by reviewing all theoretical models that attempt to explain it. We assess the generality of the mechanism upon which each model is based, and the extent to which data support its predictions. Two classes of adaptive models are identified: models that assume that the correlation arises from maternal influences on the relationship between I and offspring fitness [w(I)], and those that assume that maternal size influences the relationship between I and maternal fitness [W(I)]. The weight of evidence suggests that maternal influences on w(I) are probably not very general, and even for taxa where maternal influences on w(I) are likely, experiments fail to support model predictions. Models that assume that W(I) varies with maternal size appear to offer more generality, but the current challenge is to identify a specific and general mechanism upon which W(I) varies predictably with maternal size. Recent theory suggests the exciting possibility that a yet unknown mechanism modifies the offspring size-number trade-off function in a manner that is predictable with respect to maternal size, such that W(I) varies with size. We identify two promising avenues of inquiry. First, the trade-off might be modified by energetic costs that are associated with the initiation of reproduction ('overhead costs') and that scale with I, and future work could investigate what specific overhead costs are generally associated with reproduction and whether these costs scale with I. Second, the trade-off might be modified by virtue of condition-dependent offspring provisioning coupled with metabolic factors, and future work could investigate the proximate cause of, and generality of, condition-dependent offspring provisioning. Finally, drawing on the existing literature, we suggest that maternal size per se is not causatively related to variation in I, and the mechanism involved in the correlation is instead linked to maternal nutritional status or maternal condition, which is usually correlated with maternal size. Using manipulative experiments to elucidate why females with high nutritional status typically produce large offspring might help explain what specific mechanism underlies the maternal-size correlation.

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“…A recent study also supports the finding that size-related survival of embryos and larvae may not occur in incubation gravels of different sizes (Rollinson and Hutchings 2011), though this study was limited in scope. The present study is a more thorough test of the focal hypothesis, but we note that it has three important drawbacks, any of which may explain why we observed no pattern of size-related survival.…”

Section: Discussionmentioning

confidence: 60%

Why does egg size of salmonids increase with the mean size of population spawning gravels?

RollinsonNjal

Hutchings

2011

Can. J. Fish. Aquat. Sci.

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Population mean egg size of salmonids increases with the mean size of gravels in which a population spawns. A long-standing hypothesis is that large larvae cannot navigate small-gravel interstices, so mothers must decrease per-offspring investment when spawning gravels are small. We manipulated the size of incubation gravels and egg size of Atlantic salmon (Salmo salar) to test whether size-related entombment of larvae occurs. We find little evidence of size-related entombment, but we find evidence that gravel size does not affect all larval sizes equally. Larger larvae emerge from small gravels before development is complete and with a visible yolk sac, possibly due to oxygen limitation in small gravels. Smaller larvae always complete development in the gravel and emerge without a yolk sac. Although growth and survival may increase with juvenile size following yolk-sac absorption, juveniles with yolk sacs may fare worse when depredation rates are high. The egg size -gravel size correlation may therefore reflect increased postemergence mortality among larger offspring in smallgravel environments. Alternatively, compaction stress in fine gravels coupled with size asymmetries in larval strength may have caused the patterns that we observed, in which case our data may not help explain the egg size -gravel size correlation.Résumé : La taille moyenne des oeufs d'une population de salmonidés augmente en fonction de la taille moyenne du gravier dans lequel cette population fraie. Une hypothèse de longue date veut que les larves de grande taille ne peuvent pas se déplacer dans les interstices de gravier fin et que les mères doivent réduire leur investissement par rejeton lorsque le gravier de fraie est fin. Nous avons manipulé la taille du gravier d'incubation et la taille des oeufs chez des saumons atlantiques (Salmo salar) afin de tester s'il se produit un ensevelissement des larves en fonction de la taille. Nous trouvons peu d'indications d'un ensevelissement relié à la taille, mais il y a des preuves que la taille du gravier n'affecte pas toutes les tailles de larves de même manière. Les larves plus grandes émergent des graviers fins avant la fin de leur développement et avec un sac vitellin bien visible, peut-être à cause de la limitation de l'oxygène dans les graviers fins. Les larves plus petites complètent toujours leur développement dans le gravier et émergent sans sac vitellin. Bien que la croissance et la survie puissent augmenter en fonction de la taille des jeunes après la absorption du sac vitellin, les jeunes avec sac vitellin peuvent réussir moins bien lorsque les taux de prédation sont élevés. La corrélation entre la taille des oeufs et la taille du gravier peut donc refléter une mortalité accrue après l'émergence chez les rejetons de plus grande taille dans les environnements de gravier fin. Par ailleurs, le stress de compaction dans les graviers fins combiné aux asymétries reliées à la taille dans les forces des larves peuvent avoir causé les patrons que nous avons observés; dans ce cas, nos données pe...

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Body size-specific maternal effects on the offspring environment shape juvenile phenotypes in Atlantic salmon

Cited by 26 publications

References 70 publications

Mixed-Effects Modelling of Scale Growth Profiles Predicts the Occurrence of Early and Late Fish Migrants

Mixed-Effects Modelling of Scale Growth Profiles Predicts the Occurrence of Early and Late Fish Migrants

The positive correlation between maternal size and offspring size: fitting pieces of a life‐history puzzle

Why does egg size of salmonids increase with the mean size of population spawning gravels?

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