Predation risk shapes the degree of placentation in natural populations of live‐bearing fish

Abstract

The placenta is a complex life-history trait that is ubiquitous across the tree of life. Theory proposes that the placenta evolves in response to high performance-demanding conditions by shifting maternal investment from pre-to post-fertilisation, thereby reducing a female's reproductive burden during pregnancy. We test this hypothesis by studying populations of the fish species Poeciliopsis retropinna in Costa Rica. We found substantial variation in the degree of placentation among natural populations associated with predation risk: females from high predation populations had significantly higher degrees of placentation compared to low predation females, while number, size and quality of offspring at birth remained unaffected. Moreover, a higher degree of placentation correlated with a lower reproductive burden and hence likely an improved swimming performance during pregnancy. Our study advances an adaptive explanation for why the placenta evolves by arguing that an increased degree of placentation offers a selective advantage in high predation environments.

Parasite infestation influences life history but not boldness behavior in placental live-bearing fish

“…The degree of post-fertilization maternal provisioning in this species is extensive, with offspring increasing in dry mass more than 100-fold during gestation (MI = 117) (Reznick et al 2002 ). Moreover, P. retropinna has superfetation, the ability to carry several broods at different developmental stages (Hagmayer et al 2020 ).…”

“…P. retropinna has a particularly well-developed placenta (i.e. embryos can undergo an over 100-fold weight gain during gestation; Reznick et al 2002 ) and is often found in well-defined populations (Hagmayer et al 2020 ) making it an ideal system to study the consequences of parasitism in natural populations.…”

The Fish Family Poeciliidae as a Model to Study the Evolution and Diversification of Regenerative Capacity in Vertebrates

“…All species in the family exhibit internal fertilization and all, save for one, are viviparous (Furness et al, 2019), giving live-birth to fully developed precocial offspring (Lankheet et al, 2016). Members of this family, e.g., the guppy (Poecilia reticulata), mollies (subgenus Mollienesia), swordtails and platies (genus Xiphophorus), are commonly used in a wide variety of biological studies, ranging from cancer research and toxicology to sexual selection, life history evolution, genetics, ecology, and behavior (Ramsey et al, 2011;Pollux et al, 2014;Culumber and Tobler, 2017;Tobler et al, 2018;de Carvalho et al, 2019;McGowan et al, 2019;Thomaz et al, 2019;Hagmayer et al, 2020). This is in part because these fishes are easy to keep and breed in laboratory conditions and partly because this family provides a welldefined phylogenetic framework (Furness et al, 2019), allowing for comparative studies among closely related species with contrasting lifestyles (e.g., inhabiting different environments, displaying different forms of sexual selection, having different modes of reproduction).…”

“…Predation in particular is well-known for affecting numerous behavioral, morphological and life-history traits of Poeciliid fishes (Reznick and Endler, 1982;Reznick et al, 1990Reznick et al, , 2004O'Steen et al, 2002;Burns et al, 2009;Kotrschal et al, 2017;Hagmayer et al, 2020) and several studies have shown that the presence of predators can influence the shape and size of the caudal peduncle and fin (Gross, 1978;Winemiller, 1990;Langerhans et al, 2004;Hendry et al, 2006;Weber et al, 2012;Price et al, 2015;Hammerschlag et al, 2018). In nature fins are frequently damaged, for example as a result of disease, predator attacks, aggressive male-male conflicts or severe floods and storms (Ziskowski et al, 2008;Sinclair et al, 2011;Furness et al, 2020).…”

High Degree of Multiple Paternity and Reproductive Skew in the Highly Fecund Live-Bearing Fish Poecilia gillii (Family Poeciliidae)

“…The number of offspring a female can carry is restricted by both the limited space available in the body cavity (physical limitation; Reznick and Miles, 1989;Pires et al, 2011) and the exacerbated negative consequences of an increase in reproductive allocation on a female's swimming ability (physiological limitation; Fleuren et al, 2019;Quicazan-Rubio et al, 2019). These factors explain (at least partly) why female size is often positively correlated with brood size (Cheong et al, 1984;Reznick et al, 1992Reznick et al, , 1993Neff et al, 2008;Schrader and Travis, 2009;Hagmayer et al, 2018Hagmayer et al, , 2020: larger females can physically carry larger broods than smaller females. Simple mathematics dictate that the larger a brood, the larger the absolute number of potential sires that can contribute to that brood (Avise and Liu, 2011): i.e., a brood of two offspring can be sired by a maximum of two fathers, while a brood of 30 offspring can be sired by a maximum of 30 different males.…”