A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature

Martin, Thomas E.; Arriero, Elena; Majewska, Ania A.

doi:10.1098/rsbl.2010.1031

Cited by 33 publications

(20 citation statements)

References 18 publications

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“…However, the factors indicated above are expected to interact, especially at a broad geographical level [25,28,29], and thus detailed data from different regions are needed to understand the developmental patterns on islands.…”

Section: Discussionmentioning

confidence: 99%

Evolution of reproductive life histories in island birds worldwide

Covas¹

2011

Proc. R. Soc. B.

100

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Island environments typically share characteristics such as impoverished biotas and less-seasonal climates, which should be conducive to specific adaptations by organisms. However, with the exception of morphological studies, broad-scale tests of patterns of adaptation on islands are rare. Here, I examine reproductive patterns in island birds worldwide. Reproductive life histories are influenced by latitude, which could affect the response to insularity; therefore, I additionally test this hypothesis. Island colonizers showed mostly bi-parental care, but there was a significant increase in cooperative breeding on islands. Additionally, I found support for previous suggestions of reduced fecundity, longer developmental periods and increased investment in young on islands. However, clutch size increased with latitude at a rate nearly five times faster on the mainland than on the islands revealing a substantially stronger effect of insularity at higher latitudes. Latitude and insularity may also interact to determine egg volume and incubation periods, but these effects were less clear. Analyses of reproductive success did not support an effect of reduced nest predation as a driver of reproductive change, but this requires further study. The effect of latitude detected here suggests that the evolutionary changes associated with insularity relate to environmental stability and improved adult survival.

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Section: Discussionmentioning

confidence: 99%

Evolution of reproductive life histories in island birds worldwide

Covas¹

2011

Proc. R. Soc. B.

100

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“…For example, female European starlings (Sturnis vulgaris) were exposed to 30 min stressors four times a day for 8 days while they were incubating eggs (Cyr & Romero, 2007). In other studies, tree swallow (Tachyci netabicolour) nestlings that developed in experimentally cooled nest boxes had lower innate immune responses than nestlings from unmanipulated nest boxes (Ardia, Perez & Clotfelter, 2010; also see Nilsson, Stjemman & Nilsson, 2008;Martin, Arriero & Majewska, 2011). Stressed mothers spent more time away from their nest than unstressed mothers suggesting that incubation temperature could have been a factor that influenced offspring phenotype.…”

Section: (1) Temperature Effects On Phenotype In Wild Birdsmentioning

confidence: 99%

Ecological, evolutionary, and conservation implications of incubation temperature‐dependent phenotypes in birds

et al. 2013

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Incubation is a vital component of reproduction and parental care in birds. Maintaining temperatures within a narrow range is necessary for embryonic development and hatching of young, and exposure to both high and low temperatures can be lethal to embryos. Although it is widely recognized that temperature is important for hatching success, little is known about how variation in incubation temperature influences the post-hatching phenotypes of avian offspring. However, among reptiles it is well known that incubation temperature affects many phenotypic traits of offspring with implications for their future survival and reproduction. Although most birds, unlike reptiles, physically incubate their eggs, and thus behaviourally control nest temperatures, variation in temperature that influences embryonic development still occurs among nests within a population. Recent research in birds has primarily been limited to populations of megapodes and waterfowl; in each group, incubation temperature has substantial effects on hatchling phenotypic traits important for future development, survival, and reproduction. Such observations suggest that incubation temperature (and incubation behaviours of parents) is an important but underappreciated parental effect in birds and may represent a selective force instrumental in shaping avian reproductive ecology and life-history traits. However, much more research is needed to understand how pervasive phenotypic effects of incubation temperature are among birds, the sources of variation in incubation temperature, and how effects on phenotype arise. Such insights will not only provide foundational information regarding avian evolution and ecology, but also contribute to avian conservation.

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“…Similarly, egg temperature during incubation is strongly associated with female incubating activity (Martin ; Martin et al . ) and has recently been associated with immune activity within and across species (Ardia, Pérez & Clotfelter ; Martin, Arriero & Majewska ; DuRant et al . ).…”

Section: Discussionmentioning

confidence: 99%

“…; Martin & Schwabl ). This parentally induced variation in embryo temperatures can thereby influence development and performance of the immune system (Ardia, Pérez & Clotfelter ; Martin, Arriero & Majewska ; DuRant et al . ).…”

Section: Introductionmentioning

confidence: 99%

Ontogeny of constitutive immunity: maternal vs. endogenous influences

2013

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Summary1. Variation in ontogeny and strength of immune defence mechanisms can be integrally related to variation in life-history strategies and determined by trade-offs during development. However, little is known about the ontogeny of immune function in wild birds, especially in altricial birds and in a comparative context across altricial species with diverse life-history strategies. 2. In this study, we examined the ontogeny of constitutive immunity in a group of 22 passerine species sampled in tropical Venezuela and north temperate Arizona. 3. Our results show activity of constitutive components of the immune defence at 1-3 days posthatching and an increase in immune activity with age. Interspecific variation in immune activity at hatching was mainly explained by extrinsic factors mediated by the mother (egg size and egg temperature), suggesting an important role of maternal effects on offspring immunity at hatching. In contrast, the increase in agglutination activity with age suggests that immune function in older nestlings reflects intrinsic development. The increase in immune activity was greater in species that hatched with lower initial levels, and was somewhat negatively related to growth rate across species. 4. Our results suggest slower intrinsic development of immune function may be compensated by larger maternal contributions. Slower intrinsic development of immune function, in turn, may reflect a trade-off with faster somatic growth. Our study highlights the importance of both maternal (extrinsic) and endogenous (intrinsic) contributions to variation in immune function across altricial species that may reflect an important axis of developmental strategies.

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A trade-off between embryonic development rate and immune function of avian offspring is revealed by considering embryonic temperature

Cited by 33 publications

References 18 publications

Evolution of reproductive life histories in island birds worldwide

Evolution of reproductive life histories in island birds worldwide

Ecological, evolutionary, and conservation implications of incubation temperature‐dependent phenotypes in birds

Ontogeny of constitutive immunity: maternal vs. endogenous influences

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