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When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans.

Gillespie DO, Russell AF, Lummaa V - Proc. Biol. Sci. (2008)

Bottom Line: This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity.These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions.The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK. d.gillespie@sheffield.ac.uk

ABSTRACT
Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For 'resource-poor' landless families, but not 'resource-rich' landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

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Increased maternal fecundity leads to lower grand-offspring returns for (a) women from landless families, compared with (b) women from landowning families. In addition, increases in the proportion of offspring recruited lead to lower grand-offspring returns in both socio-economic groups. Shown are the predicted values from the minimal adequate Poisson GLMM, with a log link function and random intercepts for each parish and 10-year maternal birth cohort. Contour lines represent different numbers of grand-offspring, with the number of grand-offspring shown on the contour line. The grey shaded area gives an indication of the range of raw data points. The population mean maternal fecundity (6.61) is shown by the vertical dashed lines and the proportion of offspring recruited (0.47) by the horizontal dashed lines.
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fig2: Increased maternal fecundity leads to lower grand-offspring returns for (a) women from landless families, compared with (b) women from landowning families. In addition, increases in the proportion of offspring recruited lead to lower grand-offspring returns in both socio-economic groups. Shown are the predicted values from the minimal adequate Poisson GLMM, with a log link function and random intercepts for each parish and 10-year maternal birth cohort. Contour lines represent different numbers of grand-offspring, with the number of grand-offspring shown on the contour line. The grey shaded area gives an indication of the range of raw data points. The population mean maternal fecundity (6.61) is shown by the vertical dashed lines and the proportion of offspring recruited (0.47) by the horizontal dashed lines.

Mentions: Socio-economic status had a significant influence on the way maternal fecundity and the proportion of offspring recruited combined to predict grand-offspring number (table 2). Improved socio-economic conditions increased the number of grand-offspring gained from increased maternal fecundity (table 3). As the model in table 3 accounts for the effects of offspring recruitment, this suggests that the subsequent fecundity of offspring in landowning families remained higher than in landless families as maternal fecundity increased. This can be seen in figure 2a,b by following the horizontal dashed line, which indicates the population mean of the proportion of offspring recruited. For landowning but not landless families, the number of grand-offspring continues to increase with increasing maternal fecundity. Progressive exclusion of women with the highest fecundity confirmed that the relationship between maternal fecundity and grand-offspring number was not significantly curvilinear below seven births for landless families. Notably, this is remarkably close to the population mean maternal fecundity (6.61, s.e.±0.13). This suggests that for landless families, grand-offspring returns begin to diminish at maternal fecundities beyond the population mean. These results were qualitatively the same when we excluded from the analysis women who died before age 50, or those whose husbands died before the women reached age 50.


When fecundity does not equal fitness: evidence of an offspring quantity versus quality trade-off in pre-industrial humans.

Gillespie DO, Russell AF, Lummaa V - Proc. Biol. Sci. (2008)

Increased maternal fecundity leads to lower grand-offspring returns for (a) women from landless families, compared with (b) women from landowning families. In addition, increases in the proportion of offspring recruited lead to lower grand-offspring returns in both socio-economic groups. Shown are the predicted values from the minimal adequate Poisson GLMM, with a log link function and random intercepts for each parish and 10-year maternal birth cohort. Contour lines represent different numbers of grand-offspring, with the number of grand-offspring shown on the contour line. The grey shaded area gives an indication of the range of raw data points. The population mean maternal fecundity (6.61) is shown by the vertical dashed lines and the proportion of offspring recruited (0.47) by the horizontal dashed lines.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2366115&req=5

fig2: Increased maternal fecundity leads to lower grand-offspring returns for (a) women from landless families, compared with (b) women from landowning families. In addition, increases in the proportion of offspring recruited lead to lower grand-offspring returns in both socio-economic groups. Shown are the predicted values from the minimal adequate Poisson GLMM, with a log link function and random intercepts for each parish and 10-year maternal birth cohort. Contour lines represent different numbers of grand-offspring, with the number of grand-offspring shown on the contour line. The grey shaded area gives an indication of the range of raw data points. The population mean maternal fecundity (6.61) is shown by the vertical dashed lines and the proportion of offspring recruited (0.47) by the horizontal dashed lines.
Mentions: Socio-economic status had a significant influence on the way maternal fecundity and the proportion of offspring recruited combined to predict grand-offspring number (table 2). Improved socio-economic conditions increased the number of grand-offspring gained from increased maternal fecundity (table 3). As the model in table 3 accounts for the effects of offspring recruitment, this suggests that the subsequent fecundity of offspring in landowning families remained higher than in landless families as maternal fecundity increased. This can be seen in figure 2a,b by following the horizontal dashed line, which indicates the population mean of the proportion of offspring recruited. For landowning but not landless families, the number of grand-offspring continues to increase with increasing maternal fecundity. Progressive exclusion of women with the highest fecundity confirmed that the relationship between maternal fecundity and grand-offspring number was not significantly curvilinear below seven births for landless families. Notably, this is remarkably close to the population mean maternal fecundity (6.61, s.e.±0.13). This suggests that for landless families, grand-offspring returns begin to diminish at maternal fecundities beyond the population mean. These results were qualitatively the same when we excluded from the analysis women who died before age 50, or those whose husbands died before the women reached age 50.

Bottom Line: This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity.These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions.The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

View Article: PubMed Central - PubMed

Affiliation: Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, UK. d.gillespie@sheffield.ac.uk

ABSTRACT
Maternal fitness should be maximized by the optimal division of reproductive investment between offspring number and offspring quality. While evidence for this is abundant in many taxa, there have been fewer tests in mammals, and in particular, humans. We used a dataset of humans spanning three generations from pre-industrial Finland to test how increases in maternal fecundity affect offspring quality and maternal fitness in contrasting socio-economic conditions. For 'resource-poor' landless families, but not 'resource-rich' landowning families, maternal fitness returns diminished with increased maternal fecundity. This was because the average offspring contribution to maternal fitness declined with increased maternal fecundity for landless but not landowning families. This decline was due to reduced offspring recruitment with increased maternal fecundity. However, in landowning families, recruited offspring fecundity increased with increased maternal fecundity. This suggests that despite decreased offspring recruitment, maternal fitness is not reduced in favourable socio-economic conditions due to an increase in subsequent offspring fecundity. These results provide evidence consistent with an offspring quantity-quality trade-off in the lifetime reproduction of humans from poor socio-economic conditions. The results also highlight the importance of measuring offspring quality across their whole lifespan to estimate reliably the fitness consequences of increased maternal fecundity.

Show MeSH