Lifetime fitness consequences of early-life ecological hardship in a wild mammal population

Abstract

Early-life ecological conditions have major effects on survival and reproduction. Numerous studies in wild systems show fitness benefits of good quality early-life ecological conditions ("silver-spoon" effects). Recently, however, some studies have reported that poor-quality early-life ecological conditions are associated with later-life fitness advantages and that the effect of early-life conditions can be sex-specific. Furthermore, few studies have investigated the effect of the variability of early-life ecological conditions on later-life fitness. Here, we test how the mean and variability of early-life ecological conditions affect the longevity and reproduction of males and females using 14 years of data on wild banded mongooses (Mungos mungo). Males that experienced highly variable ecological conditions during development lived longer and had greater lifetime fitness, while those that experienced poor early-life conditions lived longer but at a cost of reduced fertility. In females, there were no such effects. Our study suggests that exposure to more variable environments in early life can result in lifetime fitness benefits, whereas differences in the mean early-life conditions experienced mediate a life-history trade-off between survival and reproduction. It also demonstrates how early-life ecological conditions can produce different selection pressures on males and females.

Keywords: early‐life; ecological variability; fitness effects; life‐history strategy; mammal; sex‐specific.

Figure 1

Banded mongooses (Mungos mungo) moving as a group and inspecting what lies ahead. Photo credit: Feargus Cooney

Figure 2

Banded mongoose mass change with age. Panel (a) shows all data and panel (b) zooms in on data from individuals between the ages of 0 and 3 years. In both panels, the vertical dotted lines divide the data into masses from individuals aged 0 to 1 year (zone i), 1 to 2 years (zone ii) and over 2 years (zone iii)

Figure 3

The rainfall pattern (a) within and (b) between years at our study site: the Mweya Peninsula, Uganda. Panel (a) shows the mean (± standard error) rainfall recorded in each month (n = 152 months, month 1 = January). Panel (b) shows the mean (filled circles and solid line) and standard deviation (open circles and dashed line) of the monthly rainfall within each year. Rainfall data for 2002 are incomplete and so not shown

Figure 4

The effect of (a) the mean and (b) the standard deviation of monthly rainfall in the past 12 months on invertebrate prey abundance. Note the log scale on the y axis

Figure 5

Male mongooses’ reproduction and survival and the mean (left‐hand panels) and variability (right‐hand panels) of rainfall in their first year. Panels show the effect on adult males’: mass (a, b), probability of siring at least one pup (c, d); in those that did sire a pup, the proportion of all pups born into their group that they sired (e, f); their lifespan (g, h); the total number of pups they sired in their lifetime (i, j). Lines show significant relationships predicted by models (see Table 3). Nonsignificant relationships are not plotted. In panel (g), the data and predicted relationships are split by into males who successfully reproduced in their lifetime (purple) and those who did not (black)

Figure 6

Graphical illustration of the hypothesized effect of changes in the (a) variability and (b) mean of early‐life rainfall on life‐history trade‐off and allocation patterns (after Saeki et al., 2014). The thin gray lines represent fitness isoclines along which all positions return an equal payoff. The thick dashed line represents the reference trade‐off slope for an individual (here straight lines for simplicity), and the yellow dot represents the reference optimal allocation of resources to survival and reproduction (where the trade‐off slope is tangential to the isocline). In panel (a), the thick red lines and dots show how an (i) increase or (ii) decrease in the variability of early‐life rainfall relaxes or increases the life‐history trade‐off constraints leading to higher or lower fitness payoffs. In panel (b), the thick blue lines and dots represent how an (iii) increase or (iv) decrease in mean early‐life rainfall leads to changes in an individual's trade‐off slope and optimal allocation of resources but no change in their overall fitness payoff