Mother’s Little Helper? The Placenta and Its Role in Intrauterine Maternal Investment in the Common Marmoset (Callithrix jacchus)

Chapter
Part of the Developments in Primatology: Progress and Prospects book series (DIPR)

Abstract

Litter size variation within the Callitrichidae is the result of complex interactions among genetic and environmental factors, and occurs across many facets of the reproductive cycle, from ovulation number to intrauterine litter size reduction to neonate lactation competition. Selection appears to have acted upon the callitrichine ability to make “decisions” relative to maternal nutritional state and litter size in a way that has yielded a highly sensitive and plastic system. Natural variation in marmoset litter size, birth weights and placental weights, and maternal condition create an opportunity to test hypotheses related to intrauterine growth retardation and maternal investment. We present evidence suggesting that differences in fetal/placental weight ratios in marmosets represent distinct strategies of intrauterine resource solicitation by members of litters of different sizes as a result of prenatal parent-offspring conflict. Individual triplets are associated with a smaller share of the placenta by weight than are twins, suggesting a mechanism by which triplets increase placental efficiency in the face of finite maternal resources and uterine space constraints. Twin and triplet fetuses appear to pursue different intrauterine strategies for maximizing allocation of the maternal resources via the placenta. Since complete triplet litters are almost never successfully reared to weaning, maternal limitations of energy intake and investment in offspring from conception to weaning appear to be in conflict with the triplet strategy of optimizing the intrauterine environment through placental development and function.

Keywords

Obesity Anemia Androgen Como Nipple 

Resumen

El tamaño de la variación entre los Callitrichidae es el resultado de una compleja interacción entre factores genéticos y de medio ambiente, y parece ocurrir a lo largo de muchas facetas del ciclo reproductivo, desde el número de ovulación a la reducción del tamaño de la fuente intrauterina a la competencia lactante del recien nacido. La selección parece haber actuado sobre la habilidad de los calitricidos de tomar “decisiones” relacionadas con el estado nutricional maternal y el tamaño de las camada en una forma que ha producido un sistema altamente sensitivo y plástico. La variación del tamaño de las camadas marmoset, sus pesos al nacer y pesos de las placentas, junto a la condición materna crearon la oportunidad de poner a prueba la hipótesis relacionada con el retraso del crecimiento intrauterino y la inversión materna. Este estudio presenta evidencias que sugieren que las diferencias en los índices de peso fetal y de placenta entre los marmosets podrían representar distintas estrategias en los recursos de incitación intrauterina por miembros de camadas de diferentes tamaños; todo ello como resultado de conflicto prenatal entre padres y descendencia. Los individuos trillizos están asociados a mayor compartimiento de la placenta que los gemelos, sugiriendo un mecanismo en el cual los trillizos solicitan crecimiento placental compensatorio en cara a recursos maternales finitos. Los fetos gemelos y trillizos parecen seguir diferentes estrategias intrauterinas para maximizar para la repartición de la placenta. Desde que las camadas de trillizos son casi nunca exitosas en la crianza durante el destete, las limitaciones maternas de energia admitida y la inversión en las crias desde la concepcion hasta el destete parecen estar en conflicto con las estrategias de los trillizos de optimizar el medio ambiente intrauterino a través del crecimiento de la placenta.

Resumo

A variação entre tamanho da prole na família Callitrichidae é o resultado de situações complexas entre fatores genéticos e ambientais e parece ocorrer por meio de muitas facetas do ciclo reprodutivo, desde o número de ovulações até a redução do tamanho da prole intra-útero e a competição dos neonatos pela lactação. A seleção parece ter atuado sobre a habilidade dos calitriquídeos de tomar “decisões” relativas ao estado nutricional materno e tamanho da prole, que resultou na produção de um sistema altamente sensível e plástico. A variação natural no tamanho da prole em sagüi, do peso ao nascimento e do peso placentário e das condições maternas cria uma oportunidade para testar hipóteses relacionadas ao retardo no crescimento intra-uterino e ao investimento materno. Nós apresentamos evidências sugerindo que as diferenças na razão peso placentário/peso fetal em sagüi podem representar diferentes estratégias de solicitação de recursos intra-uterinos pelos membros das proles de diferentes tamanhos, resultante de um conflito pais-prole durante o período pré-natal. Tendo como base o peso, indivíduos de uma prole de triplos compartilham a placenta pelo peso mais do que os gêmeos sugerindo um mecanismo pelo qual os triplos requerem um crescimento compensatório da placenta em função dos recursos finitos da mãe. Fetos duplos e triplos parecem utilizar diferentes estratégias no útero da mãe para maximizar a alocação da placenta. Uma vez que as proles de triplos quase nunca são criadas com sucesso até o desmame, as limitações da mãe na ingestão de energia e investimento na prole, da concepção ao desmame, parece gerar um conflito com as estratégias de triplos de otimizar o ambiente intra-uterino por meio do crescimento placentário.

Notes

Acknowledgments

The authors would like to thank Donna Layne Colòn, L.A.T. for her ongoing excellent management of the SNPRC marmoset colony and her skillful execution of data collection and participation in research design. Our development of this research has benefited from conversations and correspondence with Christopher Kuzawa (Northwestern University) and David Haig (Harvard University). Comments from the editors of this volume, two anonymous reviewers, and Dr. Haig have greatly improved the final manuscript. Funding for SNPRC colony management and research has been provided by NIH grants R01-RR02022 and P51-RR1396 (SDT), and grants to JNR from the American Society of Primatologists, the Center for the Integrative Study of Animal Behavior (Indiana University) and the Indiana University Graduate School Grant-in-Aid of Doctoral Research program have funded the research on which this chapter is based.

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Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  1. 1.Department of Oral Biology, College of DentistryUniversity of Illinois at ChicagoChicagoUSA

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