Martijn Hammers

Telomere length and dynamics predict mortality in a wild longitudinal study

Explaining variation in life expectancy between individuals of the same age is fundamental to our understanding of population ecology and life history evolution. Variation in the length and rate of loss of the protective telomere chromosome caps has been linked to cellular lifespan. Yet, the extent to which telomere length and dynamics predict organismal lifespan in nature is still contentious. Using longitudinal samples taken from a closed population of Acrocephalus sechellensis (Seychelles warblers) studied for over 20 years, we describe the first study into life‐long adult telomere dynamics (1–17 years) and their relationship to mortality under natural conditions (n = 204 individuals). We show that telomeres shorten with increasing age and body mass, and that shorter telomeres and greater rates of telomere shortening predicted future mortality. Our results provide the first clear and unambiguous evidence of a relationship between telomere length and mortality in the wild, and substantiate the prediction that telomere length and shortening rate can act as an indicator of biological age further to chronological age when exploring life history questions in natural conditions.

Variation in female morph frequencies and mating frequencies: random, frequency-dependent harassment or male mimicry?

Female-limited colour polymorphisms occur in a variety of species, where often one female morph (androchrome) resembles the body coloration of the conspecific male, whereas the other (gynochrome) does not. We tested predictions of two frequency-dependent hypotheses that are commonly invoked to explain the maintenance of these polymorphisms for multiple populations of the damselfly Ischnura elegans: (1) that males prefer mating with the most abundant female morph (LMR) or (2) that androchromes are functional male mimics (MM). We also asked whether variation in social and abiotic environments account for interpopulation variation in female morph frequencies. Contrary to predictions of the LMR hypothesis, morph mating frequency was not lower than expected based on morph frequency when a morph was uncommon or higher when a morph was most common. In support of the MM hypothesis, androchrome mating frequency was lower than predicted based on population morph frequency. In addition, as predicted, androchrome mating frequency increased with increasing ratio of androchromes to males, but we could not disentangle whether this was a consequence of the changing mimic/model ratio or because of rising androchrome frequency. Although variation in female morph frequencies between populations was not random across our study area, this could not be explained by geographical variation in frequencies and densities of males and females. Androchrome frequencies were higher in populations to the north and west where ambient temperatures were lower. Abiotic conditions such as temperature may need to be considered for understanding the maintenance of female-limited polymorphisms.

Age-Dependent Terminal Declines in Reproductive Output in a Wild Bird

In many iteroparous species individual fitness components, such as reproductive output, first increase with age and then decline during late-life. However, individuals differ greatly in reproductive lifespan, but reproductive declines may only occur in the period just before their death as a result of an age-independent decline in physiological condition. To fully understand reproductive senescence it is important to investigate to what extent declines in late-life reproduction can be explained by age, time until death, or both. However, the study of late-life fitness performance in natural populations is challenging as the exact birth and death dates of individuals are often not known, and most individuals succumb to extrinsic mortality before reaching old age. Here, we used an exceptional long-term longitudinal dataset of individuals from a natural, closed, and predator-free population of the Seychelles warbler (Acrocephalus sechellensis) to investigate reproductive output, both in relation to age and to the time until the death of an individual (reverse-age approach). We observed an initial age-dependent increase in reproductive output that was followed by a decline in old age. However, we found no significant decline in reproductive output in the years directly preceding death. Although post-peak reproductive output declined with age, this pattern differed between terminal and non-terminal reproductive attempts, and the age-dependence of the terminal breeding attempt explained much of the variation in age-specific reproductive output. In fact, terminal declines in reproductive output were steeper in very old individuals. These results indicate that not only age-dependent, but also age-independent factors, such as physiological condition, need to be considered to understand reproductive senescence in wild-living animals.

Reflectance spectra and mating patterns support intraspecific mimicry in the colour polymorphic damselfly Ischnura elegans

Coexistence of female colour morphs in animal populations is often considered the result of sexual conflict, where polymorphic females benefit from reduced male sexual harassment. Mate-searching males easily detect suitable partners when only one type of female is present, but become challenged when multiple female morphs coexist, which may result in frequency-dependent mate preferences. Intriguingly, in damselflies, one female morph often closely resembles the conspecific male in body coloration, which has lead to hypotheses regarding intra-specific male-mimicry. However, few studies have quantitatively evaluated the correspondence between colour reflectance spectra from males and male-like females, relying instead on qualitative visual assessments of coloration. Using colour analyses of reflectance spectra, we compared characteristics of the body coloration of ontogenetic male and female colour morphs of the damselfly Ischnura elegans. In addition, we evaluated whether males appear to (1) discriminate between immature and mature female colour morphs, and (2) whether male-like females experience reduced male mating attention and low mating frequencies as predicted from male-mimicry. Spectral reflectance data show that immature female morphs differ substantially in coloration from mature individuals. Mating frequencies were much lower for immature than mature female morphs. For the male-like female morph, measures of colour were statistically indistinguishable from that of both immature and mature conspecific males. Mating frequencies of male-like females were lower than those of other mature female morphs under field and experimental conditions. Together, our results indicate that males may use the observed spectral differences in mate choice decisions. Furthermore, male-like females may be regarded as functional mimics that have reduced attractiveness and lowered rates of sexual harassment by mate-searching males.

Senescence in the wild: Insights from a long-term study on Seychelles warblers.

Senescence--the progressive age-dependent decline in performance--occurs in most organisms. There is considerable variation in the onset and rate of senescence between and within species. Yet the causes of this variation are still poorly understood, despite being central to understanding the evolution of senescence. Long-term longitudinal studies on wild animals are extremely well-suited to studying the impact of environmental and individual characteristics (and the interaction between the two) on senescence, and can help us to understand the mechanisms that shape the evolution of senescence. In this review, we summarize and discuss the insights gained from our comprehensive long-term individual-based study of the Seychelles warbler (Acrocephalus sechellensis). This species provides an excellent model system in which to investigate the evolution of senescence in the wild. We found that Seychelles warblers show senescent declines in survival and reproduction, and discuss how individual characteristics (body condition, body size) and environmental effects (low- versus high-quality environments) may affect the onset and rate of senescence. Further, we highlight the evidence for trade-offs between early-life investment and senescence. We describe how key cellular and physiological processes (oxidative stress and telomere shortening) underpinning senescence are affected by individual and environmental characteristics in the Seychelles warbler (e.g. food availability, reproductive investment, disease) and we discuss how such physiological variation may mediate the relationship between environmental characteristics and senescence. Based on our work using Seychelles warblers as a model system, we show how insights from long-term studies of wild animals may help unravel the causes of the remarkable variation in senescence observed in natural systems, and highlight areas for promising future research.

The impact of reproductive investment and early‐life environmental conditions on senescence: support for the disposable soma hypothesis

Several hypotheses have been put forward to explain the evolution of senescence. One of the leading hypotheses, the disposable soma hypothesis, predicts a trade‐off, whereby early‐life investment in reproduction leads to late‐life declines in survival (survival senescence). Testing this hypothesis in natural populations is challenging, but important for understanding the evolution of senescence. We used the long‐term data set from a contained, predator‐free population of individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate how age‐related declines in survival are affected by early‐life investment in reproduction and early‐life environmental conditions. The disposable soma hypothesis predicts that higher investment in reproduction, or experiencing harsh conditions during early life, will lead to an earlier onset, and an increased rate, of senescence. We found that both sexes showed similar age‐related declines in late‐life survival consistent with senescence. Individuals that started breeding at a later age showed a delay in survival senescence, but this later onset of breeding did not result in a less rapid decline in late‐life survival. Although survival senescence was not directly related to early‐life environmental conditions, age of first breeding increased with natal food availability. Therefore, early‐life food availability may affect senescence by influencing age of first breeding. The disposable soma hypothesis of senescence is supported by delayed senescence in individuals that started breeding at a later age and therefore invested less in reproduction.

Ontogenetic shifts in male mating preference and morph-specific polyandry in a female colour polymorphic insect

BackgroundSexual conflict over mating rates may favour the origin and maintenance of phenotypes with contrasting reproductive strategies. The damselfly Ischnura elegans is characterised by a female colour polymorphism that consists of one androchrome and two gynochrome female morphs. Previous studies have shown that the polymorphism is genetic and to a high extent maintained by negative frequency-dependent mating success that varies temporally and spatially. However, the role of learning in male mating preferences has received little attention. We used molecular markers to investigate differences in polyandry between female morphs. In addition, we experimentally investigated innate male mating preferences and experience-dependent shifts in male mating preferences for female morphs.ResultsField and molecular data show that androchrome females were less polyandrous than gynochrome females. Interestingly, we found that naïve males showed significantly higher sexual preferences to androchrome than to gynochrome females in experimental trials. In contrast, experienced males showed no preference for androchrome females.ConclusionsThe ontogenetic change in male mate preferences occurs most likely because of learned mate recognition after experience with females, which in this case does not result in a preference for one of the morphs, but rather in the loss of an innate preference for androchrome females.

Mate-guarding intensity increases with breeding synchrony in the colonial fairy martin, Petrochelidon ariel

Extrapair paternity (EPP) is common in many socially monogamous species, influencing patterns of sexual selection and shaping many aspects of reproductive behaviour. However, factors explaining variation in the occurrence of EPP, both within and between populations, remain poorly understood. One ecological factor that has received considerable attention is breeding synchrony, but the proposed mechanisms remain contentious and the findings from the large number of correlational studies have been inconsistent. Mate guarding, a behavioural tactic to limit paternity loss, may be fundamental to any relationship between EPP and breeding synchrony. However, few studies have investigated how guarding behaviour varies with breeding synchrony, and the theoretical predictions are unclear. We examined how mate-guarding intensity in the colonial fairy martin varied with changes in breeding synchrony. To eliminate likely confounding effects of individual quality, we measured guarding intensity on multiple days during the fertile period of individual females and related this to daily variation in colony-level breeding synchrony. Similarly, we examined whether extrapair interest in fertile females varied with change in breeding synchrony. Both mate-guarding intensity and extrapair pursuit rate increased sharply several days prior to egg laying, before declining once laying commenced. When we controlled for this effect of female fertility status, guarding intensity increased with breeding synchrony. These novel findings suggest that the risk of paternity loss increases with breeding synchrony, at least among colonial species. Moreover, adjustment of guarding intensity to the risk of paternity loss may explain why most correlational studies do not reveal a relationship between EPP and breeding synchrony.

Ecological contrasts drive responses of wintering farmland birds to conservation management

In the past decades, large-scale conservation programs have been implemented to halt the decline of farmland species. The mechanisms explaining the effectiveness of these programs remain poorly understood. Here we test the recent hypothesis that the effects of conservation management are determined by the ecological contrasts in limiting resources they create relative to the baseline situation. We examine responses of wintering seed-eating farmland birds to the experimental establishment of winter food plots in areas with contrasting food availability. We found that farmland bird abundance and species richness were strongly positively related to seed availability, regardless of compositional differences between agricultural landscapes. In line with the ecological contrast hypothesis, the responses of wintering farmland birds increased with increasing conservation induced contrast in a key limiting resource. Both contrasts and relative responses were negatively related to baseline food availability, but the absolute bird density in food plots was unrelated to baseline food availability. This indicates that both relative and absolute effects of conservation management need to be considered to properly evaluate the effectiveness of conservation management.

Differences in Mating Propensity Between Immature Female Color Morphs in the Damselfly Ischnura elegans (Insecta: Odonata)

Female-limited color polymorphisms occur in a variety of animal taxa where excessive male sexual harassment may explain the coexistence of multiple female color morphs. In the color polymorphic damselfly Ischnura elegans, mature and immature female color morphs coexist at the mating site where males are in search for suitable mating partners. Here, we study male preference and female mating propensity for the two immature female morphs. As would be expected, compared to mature morphs, both immature female morphs mate much less. Within immature females, one morph consistently mates more frequently compared to the other morph, a pattern that is similar for the ontogenetically corresponding mature female morphs. Preference experiments with the two differently colored immature female morphs, however, did not indicate male mate preference for either morph. Low mating frequencies of immature females at natural sites in combination with relatively high attractiveness of immature models in terms of male preference indicate that female behavior influences female mating success.