Benefits and drawbacks of the placenta in live-bearing fish

Understanding the evolution of complex traits is of fundamental interest to scientists and non-scientists alike. The placenta is an excellent example of a complex trait that has evolved repeatedly throughout the animal kingdom. This repeated evolution and ongoing elaboration appears to point towards an adaptive advantage to specific environmental conditions; however, this potential benefit is currently insufficiently understood. In this thesis, I attempt to shed light on the causes and consequences of placental evolution by drawing on insights from the live-bearing fish family Poeciliidae.

In Chapter 2, we studied maternal causes and consequences of embryo provisioning during gestation in the placental live-bearing fish species Poeciliopsis retropinna from Costa Rica. Specifically, we examined how maternal traits (i.e. body fat, lean mass, and length) relate to pre- (allocation to eggs prior to fertilization) and post-fertilization (allocation to embryos during pregnancy) maternal provisioning and how this ultimately affects offspring size and body composition at birth. We showed that maternal traits strongly, albeit differently, correlate with embryo size and body composition throughout pregnancy. We conclude that (i) embryo size and offspring size at birth are plastic phenotypic traits predicted by the maternal phenotype, and (ii) maternal provisioning is not constant throughout pregnancy, but depends on the embryo developmental stage.

In Chapter 3, we studied natural populations of the placental live-bearing fish species P. retropinna in Costa Rica to test a key prediction of the locomotor cost hypothesis, which is that the placenta evolves in high ‘performance-demanding’ environments by gradually shifting maternal investment from pre- to post-fertilization, thereby reducing the reproductive burden experienced by females during pregnancy and improving their locomotor performance. We confirmed two key predictions of this hypothesis, which are that (i) placentas evolve in natural populations in response to high predation and (ii) that this significantly reduces a female’s reproductive burden during pregnancy. This chapter provides the first evidence for an adaptive explanation for why the placenta evolves in natural populations. Moreover, it reveals an unexpected fundamental feature of placental animals, which is that an increase in the degree of placentation can lead to a lower reproductive burden without any apparent reproductive cost: i.e. without sacrificing either fecundity or offspring size and quality at birth.

In Chapter 4, we tested the idea that placentation and superfetation reduce the reproductive burden of females during pregnancy, facilitating life in ‘performance-demanding’ (micro)habitats. If true, then placental and/or superfetatious species should be able to inhabit higher performance-demanding (micro)habitats compared to closely related non-placental and/or non-superfetatious species. For this, we used underwater visual census to study diurnal and ontogenetic microhabitat selection in Costa Rican rivers by five sympatric live-bearing fish species (family Poeciliidae) that differ in the absence/presence of placentation and superfetation. Consistent with the theory, adults of placental and superfetatious species inhabited deep and fast-flowing water, species that lack both reproductive adaptations were confined to shallow and slow-flowing areas, and species that lack a placenta but have superfetation occupied an intermediate habitat. This interspecific daytime microhabitat use was strongest in reproductive adults, intermediate in immatures, and absent in juveniles, suggesting that ontogeny influences species-specific microhabitat use. At night, all fishes, regardless of the species or age-class, congregated in shallow slow-flowing waters to rest on the river bottom. Our results suggest that placentation and superfetation may be hitherto unrecognized reproductive features that help to understand differences in ontogenetic and diurnal microhabitat preferences between sympatric live-bearing fish species.

In Chapter 5, we examined the consequences of a trematode infestation (black spot disease) in shaping life-history and boldness in the placental live-bearing fish species P. retropinna from Costa Rica. We proposed that the intimate link the placenta forms between the mother and fetus poses a risk, because parasite infestation may affect fetal growth in two non-mutually exclusive ways: (i) directly, through infestation of the developing fetus by parasites that can cross the placental barrier; and (ii) indirectly, through the modification of maternal physiology or metabolism to such an extent that it interferes with fetal development. We showed that heavily parasitized females produced smaller and worse-conditioned offspring at birth, possibly because a costly immune response during pregnancy may limit the energy available to (i) nourish developing embryos or (ii) form a well-functioning placenta. However, the infestation rate did not affect an individual’s boldness in the field. Our findings show that in placental live-bearing fish parasite infestation leads to reduced embryo provisioning during pregnancy, resulting in a smaller offspring size and quality at birth potentially with negative implications for offspring fitness.

In Chapter 6, we conducted a 7-week laboratory experiment to examine to what extent maternal food limitation during pregnancy affects offspring size and quality at birth, as well as growth and locomotor performance of offspring after birth in the placental live-bearing fish species Phalloptychus januarius. We showed that maternal food restriction resulted in a decrease in maternal wet mass throughout the experiment, leading to a reduced resource allocation to F1-offspring size and body fat, which can be compensated only in the long-term (i.e. when adult). This negatively affected the postnatal development of locomotor performance during feeding, and thus, body condition and presumably fitness after birth. This suggests that placentotrophy in poeciliids is likely a maladaptive strategy in fluctuating resource environments, because sudden reductions in maternal food availability during pregnancy result in smaller offspring with a lower locomotor performance during early life.

In Chapter 7, I put the findings of this thesis into a wider scientific context. Because superfetation is commonly found in Poeciliidae and thought to co-evolve with the evolution of the placenta, I developed an R-package to simulate the potential advantages of having superfetation, as well as both, superfetation and placentation. The simulation shows that the co-evolution of placentation and superfetation might be favored by the additive effects of both traits on the reproductive burden of females during pregnancy. Moreover, I address the potential disadvantages of having a placenta in response to various adverse environmental conditions. Finally, I present an outlook on future research by addressing possible steps and challenges to deepen the knowledge on placental evolution.