Temporal variability in offspring quality and individual reproductive output in a broadcast-spawning marine fish

Roney, Nancy E.; Oomen, Rebekah A.; Knutsen, Halvor; Olsen, Esben Moland; Hutchings, Jeffrey A.

doi:10.1093/icesjms/fsx232

Cited by 15 publications

(26 citation statements)

References 42 publications

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“…The ecotype proportions among the adult cod collected from inner and outer Risør fjord were consistent with a long-term survey of juvenile ecotype composition in this fjord system (Knutsen et al, 2018). We show that, provided the opportunity in semi-natural laboratory conditions, there is potential for substantial reproduction between cod inhabiting the inner and outer parts of Risør fjord (previously shown by Roney, Oomen, Knutsen, Olsen, & Hutchings, 2018b) and between cod of fjord and North Sea ecotype (first documented here). The range of the fjord ecotype is nearly completely overlapped by that of the North Sea ecotype in coastal areas and the presence of eggs, larvae, and adults in spawning condition has previously suggested that the North Sea cod reproduce there (Jorde, Kleiven, et al, 2018; Jorde, Synnes, et al, 2018; Knutsen et al, 2018; Rogers et al, 2014).…”

Section: Discussionmentioning

confidence: 53%

“…The multiplexes were modified from Delghandi et.al. (2003) (Multiplex 1) and Dahle et al (2006) and Glover et al (2010) (Multiplex 2), and were previously used for parental assignment of offspring from the same broodstock as that used in the present study (Roney, Oomen, Knutsen, Olsen, & Hutchings, 2018b).…”

Section: Methodsmentioning

confidence: 99%

“…Genotypes were scored using Genemapper software v.4.0 (Life Technologies). To ensure accuracy of parental genotypes, all adults were amplified three times (for details see Roney et al, 2018b), as were individuals with 3 or more missing loci or ambiguous genotypes. Individuals were independently genotyped by two (larvae) or three (adults) researchers.…”

Section: Methodsmentioning

confidence: 99%

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Cryptic microgeographic variation in responses of larval Atlantic cod to warmer temperatures

Oomen

et al. 2021

Preprint

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Although temperature is known to drive species dynamics and distributions, our understanding of the extent to which thermal plasticity varies within species is poor. Differences in plasticity can arise through local adaptation to heterogeneous environments, hybridization, and the release of cryptic genetic variation in novel environments. Here, wild Atlantic cod (Gadus morhua) from contrasting environments inside and outside of a fjord system in southern Norway spawned freely in a semi-natural laboratory environment, generating pure crosses and reciprocal hybrids. A common-garden rearing experiment of the larvae at 6°C, 9.5°C, and 13°C revealed cryptic genetic variation in thermal responses of growth and survival at warmer temperatures. Variation in growth plasticity was greatest from 9.5°C to 13°C, the latter of which exceeds temperatures currently typical of larvae in their native environments. In contrast to our prediction of intermediate hybrid responses consistent with additive genetic effects, one reciprocal hybrid cross showed a 4% increase in size at the highest temperature, whereas most crosses exhibited 4-12% reductions in size. All crosses experienced severe (76-93%) reductions in survival from 9.5°C to 13°C. Variation in survival plasticity suggests a genetically variable basis for the severity with which survival declines with increasing temperature and the potential for an adaptive response to warming. Notably, we demonstrate the potential for hybridization between coexisting 'fjord' and 'North Sea' ecotypes that naturally inhabit the inner and outer fjord environments at contrasting frequencies. Yet, ecotype explained a minor (3-10%) component of growth reaction norm variation, suggesting it is insufficient for describing important biological variation. Current broad-scale management and lack of coastal monitoring impede the development of strategies to maintain the potential for adaptation to warming temperatures in systems with such phenotypic complexity resulting from cryptic genetic variation, coexisting ecotypes, and gene flow.

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Section: Discussionmentioning

confidence: 53%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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Cryptic microgeographic variation in responses of larval Atlantic cod to warmer temperatures

Oomen

et al. 2021

Preprint

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“…Despite similarity in terms of number of individuals, average body size, sex ratio, initiation of spawning period, and body condition, cod originating from outer Risør fjord were less reproductively successful than those from inner Risør fjord, a finding consistent for both males and females. Based on data reported in a separate study (Roney, Oomen, Knutsen, Olsen, & Hutchings, ), duration of the spawning period was the same for males but longer for inner‐fjord females.…”

Section: Discussionmentioning

confidence: 99%

Fine‐scale population differences in Atlantic cod reproductive success: A potential mechanism for ecological speciation in a marine fish

Roney

Oomen

Knutsen

et al. 2018

Ecology and Evolution

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Successful resource‐management and conservation outcomes ideally depend on matching the spatial scales of population demography, local adaptation, and threat mitigation. For marine fish with high dispersal capabilities, this remains a fundamental challenge. Based on daily parentage assignments of more than 4,000 offspring, we document fine‐scaled temporal differences in individual reproductive success for two spatially adjacent (<10 km) populations of a broadcast‐spawning marine fish. Distinguished by differences in genetics and life history, Atlantic cod (Gadus morhua) from inner‐ and outer‐fjord populations were allowed to compete for mating and reproductive opportunities. After accounting for phenotypic variability in several traits, reproductive success of outer‐fjord cod was significantly lower than that of inner‐fjord cod. This finding, given that genomically different cod ecotypes inhabit inner‐ and outer‐fjord waters, raises the intriguing hypothesis that the populations might be diverging because of ecological speciation. Individual reproductive success, skewed within both sexes (more so among males), was positively affected by body size, which also influenced the timing of reproduction, larger individuals spawning later among females but earlier among males. Our work suggests that spatial mismatches between management and biological units exist in marine fishes and that studies of reproductive interactions between putative populations or ecotypes can provide an informative basis on which determination of the scale of local adaptation can be ascertained.

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“…A strategy of broadcast spawning on multiple spawning grounds, multiple times (Kjesbu, 1989 ) and over prolonged periods (Hutchings & Myers, 1994 ; Kjesbu et al, 1996 ) might act as a portfolio effect by reducing the risk of complete reproductive failure. The production of multiple egg batches within a spawning season, the number of which increases with female weight and body size (Kjesbu et al, 1996 ; Roney et al, 2018 ), could enable a batch spawner to spread the environmental risk among its offspring and mitigate the fitness consequences of environmental fluctuations. As a trade‐off in diversification, the variance in reproductive output of a multiple‐batch spawner could be lower, boosting the across‐generational geometric mean fitness, at the expense of producing a lower average number of offspring.…”

Section: Introductionmentioning

confidence: 99%

Multiple‐batch spawning as a bet‐hedging strategy in highly stochastic environments: An exploratory analysis of Atlantic cod

Hočevar

Hutchings

Kuparinen

2021

Evolutionary Applications

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Stochastic environments shape life‐history traits and can promote selection for risk‐spreading strategies, such as bet‐hedging. Although the strategy has often been hypothesized to exist for various species, empirical tests providing firm evidence have been rare, mainly due to the challenge in tracking fitness across generations. Here, we take a ‘proof of principle’ approach to explore whether the reproductive strategy of multiple‐batch spawning constitutes a bet‐hedging. We used Atlantic cod (Gadus morhua) as the study species and parameterized an eco‐evolutionary model, using empirical data on size‐related reproductive and survival traits. To evaluate the fitness benefits of multiple‐batch spawning (within a single breeding period), the mechanistic model separately simulated multiple‐batch and single‐batch spawning populations under temporally varying environments. We followed the arithmetic and geometric mean fitness associated with both strategies and quantified the mean changes in fitness under several environmental stochasticity levels. We found that, by spreading the environmental risk among batches, multiple‐batch spawning increases fitness under fluctuating environmental conditions. The multiple‐batch spawning trait is, thus, advantageous and acts as a bet‐hedging strategy when the environment is exceptionally unpredictable. Our research identifies an analytically flexible, stochastic, life‐history modelling approach to explore the fitness consequences of a risk‐spreading strategy and elucidates the importance of evolutionary applications to life‐history diversity.

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Temporal variability in offspring quality and individual reproductive output in a broadcast-spawning marine fish

Cited by 15 publications

References 42 publications

Cryptic microgeographic variation in responses of larval Atlantic cod to warmer temperatures

Cryptic microgeographic variation in responses of larval Atlantic cod to warmer temperatures

Fine‐scale population differences in Atlantic cod reproductive success: A potential mechanism for ecological speciation in a marine fish

Multiple‐batch spawning as a bet‐hedging strategy in highly stochastic environments: An exploratory analysis of Atlantic cod

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