skip to main content


Title: Longitudinal dynamics and behavioural correlates of telomeres in male wire‐tailed manakins
Abstract

Building on the predictions of state‐dependent life‐history theory, telomeres are hypothesized to either correlate with or function as an adaptive, proximate mediator of an individual's behaviour and life‐history strategy. To further understand the relationship between telomeres, behaviour and life‐history strategies, we measured male behaviour, telomere lengths and telomere dynamics in a free‐living population of known‐age, male wire‐tailed manakinsPipra filicauda.

Male wire‐tailed manakins perform coordinated displays with other males at leks and these displays form the basis of long‐term coalition partnerships. Males exhibit consistent individual differences in the number of social partners within their social network and the frequency of social interactions. Male sociality is also positively correlated with both social rise and reproductive success.

We measured male behaviour using a telemetry‐based, proximity datalogging system and blood telomere lengths were quantified using qPCR. We examined the relationships between telomere length, telomere dynamics, social status, and male behaviour. We also quantified the repeatability of telomere lengths, examined age‐related changes in telomere length, and tested for instances of telomere elongation that exceed residual error in telomere length.

Telomere length was found to be highly repeatable. More social males exhibited shorter telomeres and higher rates of telomere attrition. Telomeres did not significantly vary with age within or between individuals in either of the male social classes. Two out of 25 individuals exhibited patterns telomere elongation that exceeded residual error in telomere measurements.

Here we show that telomeres consistently vary between male wire‐tailed manakins and these differences are related to variation in male social behaviour. In this relatively long‐lived species, telomeres appear to be flexible traits that can increase or decrease in length. Overall, this study provides observational support for the hypothesis that telomeres act as a molecular marker that relates to behaviour in a state‐dependent manner. We also provide insight into the molecular consequences of individual variation in male social behaviour.

A freePlain Language Summarycan be found within the Supporting Information of this article.

 
more » « less
NSF-PAR ID:
10359838
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Functional Ecology
Volume:
35
Issue:
2
ISSN:
0269-8463
Page Range / eLocation ID:
p. 450-462
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Multiple mating by females is common and often driven by social constraints on female mate choice. However, females mate with multiple males even in systems without these social constraints and rates of multiple mating tend to be highly variable within and between populations. In lek mating systems, females are able to assess multiple males and their choice is unrestricted by pair bonds or the need for biparental care, yet some females mate with multiple males.

    To better understand the factors affecting variation in multiple mating, we investigated the occurrence of multiple paternity within clutches in a highly polygynous lek mating system.

    Using long‐term data on genetic paternity, survival, social status and individual age from a population of lance‐tailed manakinsChiroxiphia lanceolata, a species where males lek in cooperative alpha‐beta pairs, we tested five non‐exclusive hypotheses about the causes of variation in multiple mating and its benefits in females.

    We found that inexperienced males, including new alphas and rare beta sires, were disproportionately likely to share paternity when they sired any chicks. In contrast, female age (experience) was unrelated to multiple paternity. Multiple mating did not result in higher reproductive success or reduced variance in success for females, and there were neither consistently promiscuous females nor males that consistently shared paternity.

    The occurrence of multiple paternity in this lek mating system was best explained by female choice related to male characteristics that change with male experience. Our results support the hypothesis that there is a developmental component to the occurrence of multiple mating, and suggest females choose to mate multiply when their choices are not optimal.

     
    more » « less
  2. Abstract

    Telomeres, tandem repeats of TTAGGG at the ends of chromosomes, are highly dynamic structures that shorten in response to a variety of factors, including organismal stress and tissue‐specific growth rates. Cell turnover rates are frequently linked to their functions, resource availability and telomere dynamics. Using male red‐sided garter snakes,Thamnophis sirtalis parietalis, as a model, we investigated the relationship between telomere length in sperm cells, blood cells telomere length and a growth proxy (age‐adjusted body length and mass). This relationship is interesting because snakes exhibit indeterminate growth and because these garter snakes have a dissociated reproductive cycle where spermatogenesis occurs months prior to the mating season. In this study, we determined sperm telomere length (STL) and male age using qPCR and skeletochronology, respectively. Sperm telomere length correlated positively with snout–vent length (SVL) and with age‐adjusted SVL as a proxy for growth rate (residuals of size against age regression, hereafter growth), but not with age. Although an individual’s STL is correlated with blood telomere length (BTL), sperm telomeres are 60% longer than blood telomeres. In previous work, we have shown that BTL is shorter in older males and unrelated to SVL or any growth rate proxies. We hypothesized that STL is related to growth and SVL because growth and sperm production both occur during summer when resources are most abundant and stress lowest. This study is the first to compare telomere dynamics between cell types in a snake and supports growing evidence that telomere dynamics may be highly tissue‐specific and driven by the life‐history strategy of an organism.

     
    more » « less
  3. Abstract

    Many ectotherms rely on temperature cues experienced during development to determine offspring sex. The first descriptions of temperature‐dependent sex determination (TSD) were made over 50 years ago, yet an understanding of its adaptive significance remains elusive, especially in long‐lived taxa.

    One novel hypothesis predicts that TSD should be evolutionarily favoured when two criteria are met—(a) incubation temperature influences annual juvenile survival and (b) sexes mature at different ages. Under these conditions, a sex‐dependent effect of incubation temperature on offspring fitness arises through differences in age at sexual maturity, with the sex that matures later benefiting disproportionately from temperatures that promote juvenile survival.

    The American alligator (Alligator mississippiensis) serves as an insightful model in which to test this hypothesis, as males begin reproducing nearly a decade after females. Here, through a combination of artificial incubation experiments and mark‐recapture approaches, we test the specific predictions of the survival‐to‐maturity hypothesis for the adaptive value of TSD by disentangling the effects of incubation temperature and sex on annual survival of alligator hatchlings across two geographically distinct sites.

    Hatchlings incubated at male‐promoting temperatures (MPTs) consistently exhibited higher survival compared to those incubated at female‐promoting temperatures. This pattern appears independent of hatchling sex, as females produced from hormone manipulation at MPT exhibit similar survival to their male counterparts.

    Additional experiments show that incubation temperature may affect early‐life survival primarily by affecting the efficiency with which maternally transferred energy resources are used during development.

    Results from this study provide the first explicit empirical support for the adaptive value of TSD in a crocodilian and point to developmental energetics as a potential unifying mechanism underlying persistent survival consequences of incubation temperature.

    Read the freePlain Language Summaryfor this article on the Journal blog.

     
    more » « less
  4. Our understanding of state-dependent behaviour is reliant on identifying physiological indicators of condition. Telomeres are of growing interest for understanding behaviour as they capture differences in biological state and residual lifespan. To understand the significance of variable telomere lengths for behaviour and test two hypotheses describing the relationship between telomeres and behaviour (i.e. the causation and the selective adoption hypotheses), we assessed if telomere lengths are longitudinally repeatable traits related to spring migratory behaviour in captive pine siskins ( Spinus pinus ). Pine siskins are nomadic songbirds that exhibit highly flexible, facultative migrations, including a period of spring nomadism. Captive individuals exhibit extensive variation in spring migratory restlessness and are an excellent system for mechanistic studies of migratory behaviour. Telomere lengths were found to be significantly repeatable ( R = 0.51) over four months, and shorter pre-migratory telomeres were associated with earlier and more intense expression of spring nocturnal migratory restlessness. Telomere dynamics did not vary with migratory behaviour. Our results describe the relationship between telomere length and migratory behaviour and provide support for the selective adoption hypothesis. More broadly, we provide a novel perspective on the significance of variable telomere lengths for animal behaviour and the timing of annual cycle events. 
    more » « less
  5. Abstract

    Despite widespread variation in life span across species, three clear patterns exist: sex differences in life span are ubiquitous, life span is commonly traded against reproduction, and nutrition has a major influence on these traits and how they trade‐off. One process that potentially unites these patterns is intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction. If nutrient intake has sex‐specific effects on life span and reproduction but nutrient choice is genetically linked across the sexes, intralocus sexual conflict will occur and may prevent one or both sexes from feeding to their nutritional optima.

    Here we determine the potential for this process to operate in the decorated cricketGryllodes sigillatus. Using the Geometric Framework for Nutrition, we restrict male and female crickets to diets varying in the ratio of protein to carbohydrates and total nutrient content to quantify the effects on life span and daily reproductive effort in the sexes. We then use inbred lines to estimate the quantitative genetic basis of nutrient choice in males and females. We combine the nutrient effects and genetic estimates to predict the magnitude of evolutionary constraint for these traits in each sex. Finally, we present male and female crickets with a much broader range of diet pairs to determine how the sexes actively regulate their intake of nutrients.

    We show that protein and carbohydrate intake have contrasting effects on life span and reproduction in the sexes and that there are strong positive intersexual genetic correlations for the intake of these nutrients under dietary choice. This is predicted to accelerate the evolutionary response of nutrient intake in males but constrain it in females, suggesting they are losing the conflict. Supporting this view, males and females regulate nutrient intake to a common nutrient ratio that was not perfectly optimal for life span or reproduction in either sex, especially in females.

    Our findings show that intralocus sexual conflict over the optimal intake of nutrients is likely to be an important process generating sex differences in life span and reproduction and may help explain why females age faster and live shorter than males inG. sigillatus.

    A freePlain Language Summarycan be found within the Supporting Information of this article.

     
    more » « less