Getting fat or getting help? How female mammals cope with energetic constraints on reproduction

Heldstab, Sandra A.; Schaik, Carel P. van; Isler, Karin

doi:10.1186/s12983-017-0214-0

Cited by 41 publications

(43 citation statements)

References 111 publications

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“…Sex‐specific differences related to the consequences of body condition variation suggest that females and males are differentially affected. Motherhood is a significant influence in the depletion of a female's reserves for mammals (Heldstab, Schaik, & Isler, ). Our data showed a seasonal periodic decrease in SMI at the end of the wet season just after breeding.…”

Section: Discussionmentioning

confidence: 99%

Individual asymmetry as a predictor of fitness in the batCarollia perspicillata

Monteiro

Mellado

Nogueira

et al. 2019

J of Evolutionary Biology

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The measurement of fitness in wild populations is a challenging task, and a number of proxies have been proposed with different degrees of success. Developmental instability/stability (DI) is an organismal property associated with variance in bilateral asymmetry (fluctuating asymmetry—FA) and a correlated effect on fitness. This study provides evidence to corroborate the hypothesis that asymmetry partly reflects DI and is correlated with a reduction in fitness measured by survival and reproduction in bats. We studied two colonies of the bat Carollia perspicillata in southeastern Brazil over 5 years, marking and recapturing individuals. Gaussian mixture models for signed Forearm Asymmetry (ForA) distribution indicated that ~20% of asymmetry variation was due to DI heterogeneity among individuals. ForA, body condition (Scaled Mass Index—SMI) and Forearm Length (ForL) were used as predictors of survival probability in Cormack‐Jolly‐Seber models. Asymmetry was negatively associated with survival, whereas SMI and ForL were positively associated. The male C. perspicillata defend sites within the roost that are favoured by female harems, but there are mating opportunities for bachelor males, leading to both territorial disputes and sperm competition. As predicted by sexual selection, ForA was negatively associated with relative Testicle Length, a measure of reproductive potential. In females, ForA was negatively associated with the probability of two pregnancies (as opposed to one) in a given breeding season. The effect magnitudes and directions of associations suggest that asymmetry, even though not perfectly reflecting DI variation, is a useful predictor for fitness components in C. perspicillata.

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Section: Discussionmentioning

confidence: 99%

Individual asymmetry as a predictor of fitness in the batCarollia perspicillata

Monteiro

Mellado

Nogueira

et al. 2019

J of Evolutionary Biology

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“…The very conservative reproductive 507 investment may reflect the need to deal with fluctuating food abundance (Knott, 2001), 508 including multiple periods of food scarcity during the years of extended lactational effort (van 509 Noordwijk et al, 2013). The arboreal lifestyle limits opportunities for fat storage to buffer 510 fluctuations in food intake (Heldstab et al, 2017), which further contributes to the risk of 511 maternal energy depletion in orangutans (Knott, 2001, Knott et al, 2009. The slowdown also 512 enables the hypometabolism found in orangutans (Pontzer et al, 2016).…”

Section: Causes Of Mortalitymentioning

confidence: 99%

The slow ape: High infant survival and long interbirth intervals in wild orangutans

Noordwijk

Utami

Knott

et al. 2018

Journal of Human Evolution

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Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the longest average interbirth intervals of all mammals. Such slow life history can be viable only when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural conditions is expected to be extremely high. Previous estimates of orangutan life history were based on captive individuals living under very different circumstances or on small samples from wild populations. Here, we combine birth data from seven field sites, each with demographic data collection for at least 10 years (range 12-43 years) on wild orangutans to better document their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth intervals and female age at first reproduction, across species, subspecies and islands. We found an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning survival for males and females. Female survival of 94% until age at first birth (at around age 15 years) was higher than reported for any other mammal species under natural conditions. Similarly, annual survival among parous females is very high, but longevity remains to be estimated. Current data suggest no major life history differences between Sumatran and Bornean orangutans. The high offspring survival is remarkable, noting that modern human populations seem to have reached the same level of survival only in the 20th century. The orangutans' slow life history illustrates what can be achieved if a hominoid bauplan is exposed to low unavoidable mortality. Their high survival is likely due to their arboreal and non-gregarious lifestyle, and has allowed them to maintain viable populations, despite living in low-productivity habitats. However, their slow life history also implies that orangutans are highly vulnerable to a catastrophic population crash in the face of drastic habitat change. ABSTRACT 28 Orangutans (Pongo spp.) are reported to have extremely slow life histories, including the 29 longest average interbirth intervals of all mammals. Such slow life history can be viable only 30 when unavoidable mortality is kept low. Thus, orangutans' survivorship under natural 31 conditions is expected to be extremely high. Previous estimates of orangutan life history were 32 based on captive individuals living under very different circumstances or on small samples from 33 wild populations. Here, we combine birth data from seven field sites, each with demographic 34 data collection for at least 10 years (range 12-43 years) on wild orangutans to better document 35their life history. Using strict criteria for data inclusion, we calculated infant survival, interbirth 36 intervals and female age at first reproduction, across species, subspecies and islands. We found 37 an average closed interbirth interval of 7.6 years, as well as consistently very high pre-weaning 38 survival for males and females. Female survival of 94% until age at first birth (at around age 15 39 years) was higher than rep...

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“…Another factor influencing fat storage in reproduction is whether the female provides the effort alone, or has helpers. A phylogenetic analysis of 87 mammal species showed that if females have helpers, the amount of stored fat reserves called upon for reproduction is reduced (Heldstab et al, 2017).…”

Section: Introductionmentioning

confidence: 99%

The evolution of body fatness: trading off disease and predation risk

Speakman

2018

Journal of Experimental Biology

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Human obesity has a large genetic component, yet has many serious negative consequences. How this state of affairs has evolved has generated wide debate. The thrifty gene hypothesis was the first attempt to explain obesity as a consequence of adaptive responses to an ancient environment that in modern society become disadvantageous. The idea is that genes (or more precisely, alleles) predisposing to obesity may have been selected for by repeated exposure to famines. However, this idea has many flaws: for instance, selection of the supposed magnitude over the duration of human evolution would fix any thrifty alleles (famines kill the old and young, not the obese) and there is no evidence that hunter-gatherer populations become obese between famines. An alternative idea (called thrifty late) is that selection in famines has only happened since the agricultural revolution. However, this is inconsistent with the absence of strong signatures of selection at single nucleotide polymorphisms linked to obesity. In parallel to discussions about the origin of obesity, there has been much debate regarding the regulation of body weight. There are three basic models: the setpoint, settling point and dual-intervention point models. Selection might act against low and high levels of adiposity because food unpredictability and the risk of starvation selects against low adiposity whereas the risk of predation selects against high adiposity. Although evidence for the latter is quite strong, evidence for the former is relatively weak. The release from predation ∼2-million years ago is suggested to have led to the upper intervention point drifting in evolutionary time, leading to the modern distribution of obesity: the drifty gene hypothesis. Recent critiques of the dual-intervention point/ drifty gene idea are flawed and inconsistent with known aspects of energy balance physiology. Here, I present a new formulation of the dual-intervention point model. This model includes the novel suggestion that food unpredictability and starvation are insignificant factors driving fat storage, and that the main force driving up fat storage is the risk of disease and the need to survive periods of pathogen-induced anorexia. This model shows why two independent intervention points are more likely to evolve than a single set point. The molecular basis of the lower intervention point is likely based around the leptin pathway signalling. Determining the molecular basis of the upper intervention point is a crucial key target for future obesity research. A potential definitive test to separate the different models is also described.

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Getting fat or getting help? How female mammals cope with energetic constraints on reproduction

Cited by 41 publications

References 111 publications

Individual asymmetry as a predictor of fitness in the batCarollia perspicillata

Individual asymmetry as a predictor of fitness in the batCarollia perspicillata

The slow ape: High infant survival and long interbirth intervals in wild orangutans

The evolution of body fatness: trading off disease and predation risk

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