Experimental manipulation of female reproduction demonstrates its fitness costs in kangaroos

Abstract

Summary1. When resources are scarce, female mammals should face a trade-off between lactation and other life-history traits such as growth, survival and subsequent reproduction. Kangaroos are ideal to test predictions about reproductive costs because they may simultaneously lactate and carry a young, and have indeterminate growth and a long breeding season.2. An earlier study in three of our five study populations prevented female eastern grey kangaroos (Macropus giganteus) from reproducing during one reproductive season by either inserting contraceptive implants or removing very small pouch young. We explored how individual and environmental variables affect the costs of reproduction over time, combining this experimental reduction of reproductive effort with multi-year monitoring of 270 marked females. Experimental manipulation should control for individual heterogeneity, revealing the costs of reproduction and their likely sources. We also examined the fitness consequences of reproductive effort and offspring sex among unmanipulated individuals to test whether sex allocation strategies affected trade-offs. 3. Costs of reproduction included longer inter-birth intervals and lower probability of producing a young that survived to 7 months in the subsequent reproductive event. Weaning success, however, did not differ significantly between manipulated and control females. By reducing reproductive effort, manipulation appeared to increase individual condition and subsequent reproductive success. 4. Effects of offspring sex upon subsequent reproductive success varied according to year and study population. Mothers of sons were generally more likely to have a young that survived to 7 months, compared to mothers of daughters. 5. The fitness costs of reproduction arise from constraints in both acquisition and allocation of resources. To meet these costs, females delay subsequent parturition and may manipulate offspring sex. Reproductive tactics thus vary according to the amount of resource available to each individual, promoting a wide range in reproductive performance within and among individuals and populations.

Long‐term studies of bighorn sheep and mountain goats reveal fitness costs of reproduction

“…In feral sheep ( Ovis aries ), contraceptive implants increased female survival, but did not improve subsequent breeding performance (Tavecchia et al, ). In Eastern grey kangaroos ( Macropus giganteus ), females prevented from reproducing for one year subsequently gave birth earlier and their offspring had higher survival compared with control females (Gélin, Wilson, Coulson, & Festa‐Bianchet, ).…”

Somatic growth contributes to population variation in marine fishes

“…Indirect consequences of somatic growth variation include changes in reproductive rate, as fecundity increases with body size (Hendry, Day, & Cooper, ; Sæther, ), or mortality, as smaller individuals are more vulnerable to predation (Lima, ; McNamara & Houston, ). Indirect effects on fecundity could be amplified as decreased growth rates may delay maturity (Hutchings, ; Stearns & Koella, ) and individuals also modify fecundity in response to environmental conditions across life‐history strategies, from fast‐growing salmonids (Kindsvater, Alonzo, Mangel, & Bonsall, ) to slow‐growing marsupials (Gélin, Wilson, Coulson, & Festa‐Bianchet, ). Alteration of population age structure may govern how population dynamics respond to changes in vital rates (Caswell, Nisbet, Roos, & Tuljapurkar, ).…”

Individual quality and age but not environmental or social conditions modulate costs of reproduction in a capital breeder

“…In long-lived capital breeders, mothers usually favor their own growth and body maintenance over that of their offspring, resulting in negligible costs on an individual's own survival Hamel, Cote, & Festa-Bianchet, 2010). Nonetheless, reproduction can still reduce a mother's body condition (Gélin, Wilson, Coulson, & Festa-Bianchet, 2015;Monteith et al, 2013;Simard, Huot, de Bellefeuille, & Cote, 2014;Testa & Adams, 1998) and future reproductive success (Festa-Bianchet, Gaillard, & Jorgenson, 1998;Hamel, Gaillard et al, 2010;Moyes et al, 2011). Moreover, costs of reproduction can be influenced by a complex interplay among numerous intrinsic, environmental, and social factors (e.g., Hamel, Cote et al, 2010;Lescroel, Dugger, Ballard, & Ainley, 2009;Rauset, Low, & Persson, 2015;Robert, Paiva, Bolton, Jiguet, & Bried, 2012).…”

“…Life-history trade-offs including costs of reproduction can be difficult to discern and explain in the presence of persistent amongindividual differences in performance-commonly referred to as "individual quality" (Cam, Link, Cooch, Monnat, & Danchin, 2002;Clutton-Brock, 1984;Gélin et al, 2015;Weladji et al, 2008;Wilson & Nussey, 2010)-or in the context of short-term or local environmental effects (Hamel, Yoccoz, & Gaillard, 2014). Variation in quality can have environmental (McNamara, 1998) or genetic (Nussey, Postma, Gienapp, & Visser, 2005) origins.…”