The evolution of placentas and superfetation in the fish genus Poecilia (Cyprinodontiformes: Poeciliidae: subgenera Micropoecilia and Acanthophacelus)

Abstract

Complex adaptations are often found in nature, although our ability to discern how and why such traits evolved is limited because their origin occurred in the distant past and the details of their evolution have been lost through extinction (e.g. all placental mammals inherited their placentas from a single common ancestor that lived over 100 Mya). In poeciliid fishes, placentas have evolved independently multiple times and portions of the path to the evolution of complexity can be found in living species. In the present study, we describe the life histories of six species within the genus Poecilia that includes the subgenera Micropoecilia and Acanthophacelus (the guppy; Poecilia reticulata). We demonstrate that extensive placentotrophy and superfetation, the ability to simultaneously carry more than one developing brood, have evolved within this clade. These fish represent the third clade in which we have discovered the independent origin of a placenta that also includes close relatives that lack a placenta. We discuss possible adaptive advantages of the joint evolution of extensive placentation and superfetation in these fishes.

Spatial and temporal variation in superfoetation and related life history traits of two viviparous fishes: Poeciliopsis gracilis and P. infans

“…However, sampling errors in classification have led to erroneous mapping of the trait onto phylogenies. For example, Pires et al (2010) recently found superfoetation in the lineage composed of Poecilia bifurca, P. branneri and P. parae, and this represents an additional independent origin of superfoetation that was previously unknown. In addition, more information is needed to clarify the spatial and temporal variation in this reproductive trait.…”

“…For instance, in their comprehensive summary of life histories within the family Poeciliidae, Reznick and Miles (1989) classified species as either superfoetating or non-superfoetating. Yet, ignoring intraspecific variation did lead to incorrect classifications; these authors put down Poecilia parae as nonsuperfoetating, but a subsequent study showed that females sometimes bear simultaneous broods (Pires et al 2010), a finding that revealed an additional independent evolutionary origin of superfoetation (Meredith et al 2011). Even repeated sampling, if limited, can lead to an underestimate of the number of species that undergo superfoetation.…”

“…In the laboratory, Travis et al (1987) found that female H. formosa experimentally given high food levels had a significantly greater incidence of superfoetation than females given restricted amounts of food, whereas Pires et al (2007) found differences in the degree of superfoetation exhibited by two distinct populations of Poeciliopsis prolifica in captivity. In the field, population differences in superfoetation have been reported in P. baenschi (Molina-Moctezuma 2011), Poecilia branneri (Pires et al 2010) and Poeciliopsis turrubarensis, which produce more simultaneous broods (and are thus more streamlined) in fast-than in slow-flowing streams (Zúñiga-Vega et al 2007), whereas seasonal intrapopulation differences in superfoetation have been documented only in H. formosa (Travis et al 1987;Leips and Travis 1999). As the limited number of the above examples indicates, evidence of intraspecific variation in superfoetation is scarce (Johnson and Bagley 2011).…”

“…Superfoetation is common in viviparous fishes (Turner 1937;Scrimshaw 1944;Thibault and Schultz 1978) and has been reported in at least three unrelated families: Clinidae (Gunn and Thresher 1991), Zenarchopteridae and Poeciliidae (Reznick and Miles 1989;Reznick et al 2007). Within the Poeciliidae, superfoetation occurs in several genera such as Poeciliopsis, Heterandria, Neoheterandria (Reznick and Miles 1989;Reznick et al 1992;Pollux et al 2009) and Poecilia (subgenus Micropoecilia; Pires et al 2010), whereas other genera do not include superfoetating species (e.g. Belonesox, Brachyrhaphis and Xiphophorus; Reznick and Miles 1989;Pollux et al 2009).…”

Monophyly of Heterandriini (Teleostei: Poeciliidae) revisited: a critical review of the data

“…Poeciliids are characterized by a suite of derived characters including the position of the pectoral fins high on side of the body, an anterior placement of the pelvic fins ventral to the pectoral fins, the presence of pleural ribs on the first several haemal arches, a bony cap on the ventral hypohyal lying over the anterior facet of the anterior ceratohyal, and supraorbital laterosensory pores with neuromasts embedded in fleshy grooves (Ghedotti, 2000). Despite the widespread use of poeciliid fishes in ecological and evolutionary studies (e.g., Rauchenberger, 1990;Meyer et al, 1994;Borrowsky et al, 1995;Marcus & McCune, 1999;Spencer et al, 1999;Spencer et al, 2000;Morris et al, 2001;Kallman et al, 2004;Gutierrez-Rodriguez et al, 2007a, 2007bReznick et al, 2007;Leberg & Firmin, 2008;Purcell et al, 2008;Martin et al, 2009;Pollux et al, 2009;Meredith et al, 2010;Pires et al, 2010;Albert & Johnson, 2011), the phylogenetic interrelationships among poeciliid species remain incompletely resolved.The family Poeciliidae comprises three subfamilies that are restricted to fresh and brackish continental waters: Poeciliinae, Procatopodinae, and Aplocheilichthyinae (Ghedotti, 2000;Lucinda, 2003;Hrbek et al, 2007). The Poeciliinae includes at least 228 species distributed across much of the tropical and subtropical portions of the Americas, from the La Plata estuary of northern Argentina to southeastern United States, with species richness reaching a zenith in Middle America and the West Indies (Rosen & Bailey, 1963;Lucinda, 2003;Hrbek et al, 2007;.…”