Increased superfetation precedes the evolution of advanced degrees of placentotrophy in viviparous fishes of the family Poeciliidae

Abstract

The causes and consequences of the evolution of placentotrophy (post-fertilization nutrition of developing embryos of viviparous organisms by means of a maternal placenta) in non-mammalian vertebrates are still not fully understood. In particular, in the fish family Poeciliidae there is an evolutionary link between placentotrophy and superfetation (ability of females to simultaneously bear embryos at distinct developmental stages), with no conclusive evidence for which of these two traits facilitates the evolution of more advanced degrees of the other. Using a robust phylogenetic comparative method based on Ornstein–Uhlenbeck models of adaptive evolution and data from 36 poeciliid species, we detected a clear causality pattern. The evolution of extensive placentotrophy has been facilitated by the preceding evolution of more simultaneous broods. Therefore, placentas became increasingly complex as an adaptive response to evolutionary increases in the degree of superfetation. This finding represents a substantial contribution to our knowledge of the factors that have shaped placental evolution in poeciliid fishes.

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royalsocietypublishing.org/journal/rsbl
Research
Cite this article: García-Cabello KN, Fuentes-
González JA, Saleh-Subaie N, Pienaar J,
Zúñiga-Vega JJ. 2022 Increased superfetation
precedes the evolution of advanced degrees of
placentotrophy in viviparous fishes of the
family Poeciliidae. Biol. Lett. 18: 20220173.
https://doi.org/10.1098/rsbl.2022.0173
Received: 31 March 2022
Accepted: 9 September 2022
Subject Areas:
evolution
Keywords:
lecithotrophy, matrotrophy, placentas,
simultaneous broods, viviparity
Author for correspondence:
J. Jaime Zúñiga-Vega
e-mail: jzuniga@ciencias.unam.mx
Electronic supplementary material is available
online at https://doi.org/10.6084/m9.figshare.
c.6214711.
Evolutionary biology
Increased superfetation precedes the
evolution of advanced degrees of
placentotrophy in viviparous fishes of the
family Poeciliidae
Karla N. García-Cabello
1
, Jesualdo A. Fuentes-González
4
, Nabila Saleh-Subaie
2
,
Jason Pienaar
5
and J. Jaime Zúñiga-Vega
3
1
Posgrado en Ciencias del Mar y Limnología,
2
Programa de Doctorado en Ciencias Biomédicas, and
3
Departamento de Ecología y Recursos Naturales, Facultad de Ciencias, Universidad Nacional Autónoma de
México, Ciudad de México 04510, Mexico
4
Department of Biological Sciences, University of Alabama, Tuscaloosa, AL 35487, USA
5
Department of Biological Sciences, Florida International University, Miami, FL 33199, USA
KNG-C, 0000-0002-1077-7265; JJZ-V, 0000-0002-9661-1521
The causes and consequences of the evolution of placentotrophy (post-
fertilization nutrition of developing embryos of viviparous organisms by
means of a maternal placenta) in non-mammalian vertebrates are still not
fully understood. In particular, in the fish family Poeciliidae there is an
evolutionary link between placentotrophy and superfetation (ability of females
to simultaneously bear embryos at distinct developmental stages), with no con-
clusive evidence for which of these two traits facilitates the evolution of more
advanced degrees of the other. Using a robust phylogenetic comparative
method based on Ornstein–Uhlenbeck models of adaptive evolution and data
from 36 poeciliid species, we detected a clear causality pattern. The evolution
of extensive placentotrophy has been facilitated by the preceding evolution of
more simultaneous broods. Therefore, placentas became increasingly complex
as an adaptive response to evolutionary increases in the degree of superfetation.
This finding represents a substantial contribution to our knowledge of the factors
that have shaped placental evolution in poeciliid fishes.
1. Introduction
Non-mammalian placentas have received considerable attention during the
past two decades because their natural diversity and multiple independent ori-
gins have triggered questions about the factors shaping the evolution of these
astonishing reproductive structures [1]. A placenta is an organ formed through
the intimate apposition of fetal and maternal tissues for physiological exchange
[2]. In some groups of viviparous fishes and reptiles, the anatomical structure of
their placentas varies substantially among closely related species [3,4]. Studies
comparing some of these species have demonstrated that the amount of nutri-
ents that females actively transfer to their developing embryos after fertilization
by means of their placentas (known as placentotrophy [1]) is positively corre-
lated with the degree of complexity of their placental tissues [4–6]. Thus,
advanced degrees of placentotrophy are possible by means of thickened placen-
tal cells with numerous enlarged vesicles, abundant microvilli and richly
supplied with capillaries (in particular of the maternal portion of the placenta;
[4,5]). By contrast, lecithotrophy is a developmental pattern in which yolk of the
ovum (provided by the female before fertilization) represents the main source
of embryonic nutrition [1,7]. In several viviparous species, lecithotrophy is
associated with simpler placentas that primarily provide the basic function of
© 2022 The Author(s) Published by the Royal Society. All rights reserved.