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.

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Multiple paternity is a common phenomenon within the live-bearing fish family Poeciliidae. There is a great variety in brood sizes of at least two orders-of-magnitude across the family. However, little is known about the ramifications of this remarkable variation for the incidence and degree of multiple paternity and reproductive skew. Mollies (subgenus Mollienesia, genus Poecilia) produce some of the largest broods in the family Poeciliidae, making them an excellent model to study the effects of intraspecific variation in brood size on patterns of multiple paternity. We collected samples of the live-bearing fish Poecilia gillii from 9 locations in Costa Rica. We measured body size of 159 adult females, of which 72 were pregnant. These samples had a mean brood size of 47.2 ± 3.0 embryos, ranging from 4 to 130 embryos. We genotyped 196 field-collected specimens with 5 microsatellite markers to obtain location-specific allele frequencies. In addition, we randomly selected 31 pregnant females, genotyped all their embryos (N = 1346) and calculated two different parameters of multiple paternity: i.e., the minimum number of sires per litter using an exclusion-based method (GERUD) and the estimated number of sires per litter using a maximum likelihood approach (COLONY). Based on these two approaches, multiple paternity was detected in 22 and 27 (out of the 31) females, respectively, with the minimum number of sires ranging from 1 to 4 (mean ± SE: 2.1 ± 0.16 sires per female) and the estimated number of fathers ranging from 1 to 9 (mean ± SE: 4.2 ± 0.35 sires per female). The number of fathers per brood was positively correlated with brood size, but not with female size. Next, we calculated the reproductive skew per brood using the estimated number of sires, and found that in 21 out of the 27 multiply sired broods sires did not contribute equally to the offspring. Skew was not correlated with either female size, brood size or the number of sires per brood. Finally, we discuss several biological mechanisms that may influence multiple paternity and reproductive skew in P. gillii as well as in the Poeciliidae in general.

Superfetation, the ability to carry several overlapping broods at different developmental stages, has evolved independently multiple times within the live-bearing fish family Poeciliidae. Even though superfetation is widespread among poeciliids, its evolutionary advantages remain unclear. Theory predicts that superfetation should increase polyandry by increasing the probability that temporally overlapping broods are fertilized by different fathers. Here, we test this key prediction in two poeciliid species that each carry two temporally overlapping broods: Poeciliopsis retropinna and P. turrubarensis. We collected 25 females per species from freshwater streams in South-Eastern Costa Rica and assessed multiple paternity by genotyping all their embryos (420 embryos for P. retropinna; 788 embryos for P. turrubarensis) using existing and newly developed microsatellite markers. We observed a high frequency of unique sires in the simultaneous, temporally overlapping broods in P. retropinna (in 56% of the pregnant females) and P. turrubarensis (79%). We found that the mean number of sires within females was higher than the number of sires within the separate broods (2.92 sires within mothers vs. 2.36 within separate broods in P. retropinna; and 3.40 vs 2.56 in P. turrubarensis). We further observed that there were significant differences in the proportion of offspring sired by each male in 42% of pregnant female P. retropinna and 65% of female P. turrubarensis; however, this significance applied to only 9% and 46% of the individual broods in P. retropinna and P. turrubarensis, respectively, suggesting that the unequal reproductive success of sires (i.e. reproductive skew) mostly originated from differences in paternal contribution between, rather than within broods. Together, these findings tentatively suggest that superfetation may promote polyandry and reproductive skew in live-bearing fishes.

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