Alberto Velando

Senescent birds redouble reproductive effort when ill: confirmation of the terminal investment hypothesis

This study reports an experimental confirmation of the terminal investment hypothesis, a longstanding theoretical idea that animals should increase their reproductive effort as they age and their prospects for survival and reproduction decline. Previous correlational and experimental attempts to test this hypothesis have yielded contradictory results. In the blue-footed booby, Sula nebouxii, a long-lived bird, after initial increase, male reproductive success declines progressively with age. Before laying, males of two age classes were challenged with lipopolysaccharide to elicit an immune response, which induced symptoms of declining survival prospects. Reproductive success of immune-challenged mature males fell, while that of immune-challenged old males showed a 98% increase. These results demonstrate that senescent males with poor reproductive prospects increase their effort when those prospects are threatened, whereas younger males with good reproductive prospects do not.

Avoiding bad genes: oxidatively damaged DNA in germ line and mate choice

August Weismann proposed that genetic changes in somatic cells cannot pass to germ cells and hence to next generations. Nevertheless, evidence is accumulating that some environmental effects can promote heritable changes in the DNA of germ cells, which implies that some somatic influence on germ line is possible. This influence is mostly detrimental and related to the presence of oxidative stress, which induces mutations and epigenetic changes. This effect should be stronger in males due to the particular characteristics of sperm. Here, we propose the hypothesis that females are able to avoid males with oxidatively damaged DNA in the germ line by using oxidative-dependent (pre- and post-mating) signals. This new hypothesis may shed light on unsolved questions in evolutionary biology, such as the benefits of polyandry, the lek paradox, or the role of sexual selection on the evolution of aging.

Pre-fledgling oxidative damage predicts recruitment in a long-lived bird

Empirical evidence has shown that stressful conditions experienced during development may exert long-term negative effects on life-history traits. Although it has been suggested that oxidative stress has long-term effects, little is known about delayed consequences of oxidative stress experienced early in life in fitness-related traits. Here, we tested whether oxidative stress during development has long-term effects on a life-history trait directly related to fitness in three colonies of European shags Phalacrocorax aristotelis. Our results revealed that recruitment probability decreased with oxidative damage during the nestling period; oxidative damage, in turn, was related to the level of antioxidant capacity. Our results suggest a link between oxidative stress during development and survival to adulthood, a key element of population dynamics.

Senescence of Maternal Effects: Aging Influences Egg Quality and Rearing Capacities of a Long‐Lived Bird

Senescence could depress prenatal and postnatal capacities of mothers to invest in offspring. Longitudinal observations on the blue‐footed booby (Sula nebouxii) revealed a quadratic effect of female age on fledgling production and cohort differences in rate of reproductive decline. By swapping clutches between females of different ages, we tested whether reproductive senescence is due to decline in egg quality or capacity to care. As laying mothers aged, egg size, ulna length of 5‐day‐old chicks, and ulna growth of second chicks up to age 30 days declined, and as rearing mothers aged, ulna growth and cellular mediated immune response of second chicks diminished. Oddly, senescent females (>11 years) produced more fledglings when rearing offspring of middle‐aged females (8–11 years) than when rearing offspring of senescent or young females. Thus, senescence reduced egg quality and rearing capacities, and reproductive success of senescent mothers depended on prenatal effects associated with the age of the laying mother. Reproductive senescence of boobies may involve constraints on resources allocated to reproduction as well as adaptive adjustment of provision and care according to offspring value, implying that negative effects of senescence on offspring survival can be ameliorated by plasticity in postlaying or postnatal care.

Pigment allocation to eggs decreases plasma antioxidants in a songbird

Although evidence is accumulating on the adaptive function of female ornamentation, very little is known about maternal allocation decisions involving sexual signaling and other reproductive functions. Blue egg coloration has been suggested as a sexually selected signal of female quality to males, and some recent studies are in accordance with this hypothesis. Blue eggshell coloration results from the deposition of biliverdin pigment by laying females, which is a potent antioxidant. Thus, egg pigmentation should be costly in terms of antioxidants, an assumption of the signaling hypothesis that has not been tested yet. We induced increased reproductive effort in a set of female pied flycatchers Ficedula hypoleuca through nest removal and measured egg pigmentation and plasma antioxidant levels in relation with a control group. Experimental females showed a negative association between egg color and plasma antioxidant levels, while there was no relationship for control birds. This supports that egg pigmentation is costly in terms of general antioxidant defenses and suggests a tradeoff between the allocations to both traits. Furthermore, experimental females with more colorful eggs raised more fledglings, especially when breeding early. Controls did not show a relationship between egg color and reproductive success. Females laying more colorful eggs could have shifted their allocation decisions towards current reproduction, at the expense of their own antioxidant defenses. Our results highlight that blue egg coloration is a life-history trait, subject to tradeoffs with other attributes, and seems to be especially informative under harsh breeding conditions.

Effects of recruiting age on senescence, lifespan and lifetime reproductive success in a long-lived seabird

Theories of ageing predict that early reproduction should be associated with accelerated reproductive senescence and reduced longevity. Here, the influence of age of first reproduction on reproductive senescence and lifespan, and consequences for lifetime reproductive success (LRS), were examined using longitudinal reproductive records of male and female blue-footed boobies (Sula nebouxii) from two cohorts (1989 and 1991). The two sexes showed different relationships between age of first reproduction and rate of senescent decline: the earlier males recruited, the faster they experienced senescence in brood size and breeding success, whereas in females, recruiting age was unrelated to age-specific patterns of reproductive performance. Effects of recruiting age on lifespan, number of reproductive events and LRS were cohort- and/or sex-specific. Late-recruiting males of the 1989 cohort lived longer but performed as well over the lifetime as early recruits, suggesting the existence of a trade-off between early recruitment and long lifespan. In males of the 1991 cohort and females of both cohorts, recruiting age was apparently unrelated to lifespan, but early recruits reproduced more frequently and fledged more chicks over their lifetime than late recruits. Male boobies may be more likely than females to incur long-term costs of early reproduction, such as early reproductive senescence and diminished lifespan, because they probably invest more heavily than females. In the 1991 cohort, which faced the severe environmental challenge of an El Niño event in the first year of life, life-history trade-offs of males may have been masked by effects of individual quality.

Brainless but not clueless: earthworms boost their ejaculates when they detect fecund non-virgin partners

In many animals in which females store sperm, males may detect female mating status and, in order to outcompete rival sperm, increase ejaculate size when copulating with non-virgin females. Although most studies have been restricted to organisms with separate sexes, theoretical models suggest that sperm competition should also be an important selective agent shaping life-history traits in simultaneous hermaphrodites. Nevertheless, the empirical support for ejaculate adjustment in a mating opportunity is scarce in hermaphrodites. In the present study, we performed a double-mating experiment to determine whether earthworms (Eisenia andrei) detect the mating status of their partners and whether they respond by adjusting their ejaculate. We found that earthworms triplicated the donated sperm when mating with a non-virgin mate. Moreover, such increases were greater when the worms were mated with larger (more fecund) partners, indicating that earthworms perform a fine-tune control of ejaculate volume. The results of the present study suggest that, under high intensity of sperm competition, partner evaluation is subject to intense selection in hermaphrodite animals, and donors are selective about to whom they donate how much sperm.

Population trends and reproductive success of the European shag Phalacrocorax aristotelis on the Iberian Peninsula following the Prestige oil spill

In 2003, immediately following the Prestige oil spill in Galicia, Spain, we studied the population trends and reproductive performance of European shags (Phalacrocorax aristotelis) at oiled and unoiled colonies. This bird is an important member of the nearshore marine community, breeding in the area affected by the Prestige oil spill. The European shag feeds around the breeding colonies throughout the year, making it a useful indicator of environmental change. Before the oil spill, population trends were similar between oiled and unoiled colonies. Nevertheless, colonies located within the path of the oil suffered greater declines (ca. 10%) compared with pre-spill trends and with population trends at unoiled colonies. In 2003, the breeding success was 50% lower in oiled colonies compared with unoiled colonies. The data available from pre-spill years suggest that the annual reproductive success did not differ among colonies before the impact. European shags breeding at colonies affected by oil showed a negative initial impact from the Prestige oil spill. The reduction in reproductive success at oiled colonies may be due to sub-lethal effects of oil exposure or low food availability after the oil spill.

Parental age and lifespan influence offspring recruitment: a long-term study in a seabird.

Recent studies of wild populations provide compelling evidence that survival and reproduction decrease with age because of senescence, a decline in functional capacities at old ages. However, in the wild, little is known about effects of parental senescence on offspring quality. We used data from a 21-year study to examine the role of parental age on offspring probability of recruitment in a long-lived bird, the blue-footed booby (Sula nebouxii). Offspring probability of recruiting into the breeding population varied over the life of parents and effects age were similar in mothers and fathers. Offspring recruitment was high when parents were roughly 6–12 years old and low before and after then. Effects of parental age on offspring recruitment varied with lifespan (parental age at last reproduction) and previous breeding experience. Offspring recruitment from young and old parents with long reproductive lifespans was greater than that of offspring from parents with short lifespans at young and old ages. For parents with little previous breeding experience recruitment of offspring decreased with their hatch date, but experienced parents were no similarly affected. We found evidence of terminal effects on offspring recruitment in young parents but not in older parents, suggesting that senescence is more likely a gradual process of deterioration than a process of terminal illness. Failure to recruit probably reflects mortality during the first years after independence but also during the fledgling transition to full independence. Our results show effects of parental age and quality on offspring viability in a long-lived wild vertebrate and support the idea that wild populations are composed of individuals of different quality, and that this individual heterogeneity can influence the dynamics of age-structured populations.

Biliverdin-based egg coloration is enhanced by carotenoid supplementation

Avian eggshell color is remarkably variable among and within species and its possible function has long been controversial. Female birds use biliverdin pigment to color their eggs blue and green. Although evidence is accumulating that blue-green eggshell coloration is costly to produce, the exact mechanisms underlying its expression are little studied. Biliverdin pigment is involved in important maintenance functions such as immune and antioxidant defenses and shows similar properties to carotenoid pigments. Carotenoids play a role as immunoenhancers and have the potential to ameliorate the impact of oxidative processes, although their antioxidant function could be minor for some bird species. Important life-history components can be limited by carotenoid availability, including sexual displays and fecundity. Here we explored if biliverdin-based eggshell pigmentation was affected by carotenoid availability in a seabird, by performing a carotenoid supplementation experiment in female blue-footed boobies (Sula nebouxii) after laying their first egg. In this species, blue eggshell color is associated with incubation patterns, and carotenoid availability affects the crucial trade-off between female foot ornamentation and fecundity. We found that under natural conditions, there was a decline in eggshell color with laying order, suggesting pigment limitation for females. However, carotenoid-supplemented females had enhanced second egg coloration compared to controls, and the color increase was independent of their previous pigment allocation to the first egg. Our results suggest that biliverdin-based eggshell coloration is costly to produce and can be alleviated by current carotenoid availability.