Evolution of viviparity: what can Australian lizards tell us?

Thompson, Michael B.; Stewart, James R.; Speake, Brian K.; Hosie, Margot J.; Murphy, Christopher R.

doi:10.1016/s1096-4959(02)00013-1

Cited by 43 publications

(33 citation statements)

References 56 publications

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“…and viviparity, because some species exhibit oviparity (egg laying), whereas others are viviparous (live bearing) with chorioallantoic placentae ranging from simple (Weekes, 1935) to complex (Thompson et al, 2002).…”

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Claudin‐5 is Restricted to the Tight Junction Region of Uterine Epithelial Cells in the Uterus of Pregnant/Gravid Squamate Reptiles

Biazik

Thompson

Murphy

2008

The Anatomical Record

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Claudin-5, a tight junctional protein associated with ion and size selectivity, has been found in the uterus of skinks. This study has generated critical information about the molecular assembly of the tight junction at various stages of the reproductive cycle in the skink uterus. Recent studies looking at tight junctional proteins found occludin expression in the tight junction region of uterine epithelial cells in the skink uterus; however, occludin did not disclose any further information about the ions and size of ions permeating across the paracellular pathway. A 22-kDa claudin-5 band was detected in the uterus of the skinks present in this study and immunohistochemistry revealed that claudin-5 redistributes to the tight junction region of the lateral plasma membrane of uterine epithelial cells in late stage pregnancy/gravidity. This finding indicates that the tight junction becomes more assembled to precisely regulate ion and solute permeation in late stage pregnancy/gravidity. Claudin-5 with its functional role as a molecular sieve due to the formation of ion and size selective pores suggests that permeation of ions smaller than 0.8 kDa are restricted when claudin-5 is redistributed to the tight junction region of the later plasma membrane. This report is the first description of the molecular mechanisms that may be involved in regulating nutrient provision in the reptilian uterus.

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Claudin‐5 is Restricted to the Tight Junction Region of Uterine Epithelial Cells in the Uterus of Pregnant/Gravid Squamate Reptiles

Biazik

Thompson

Murphy

2008

The Anatomical Record

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“…In addition, its phylogenetic and biogeographic history is well-studied Mateos, 2005). Moreover, species in this genus vary in important reproductive traits: their degree of superfetation (the number of distinct developing broods found simultaneously within a female) and the presence of either lecithotrophy or different degrees of placentotrophy (quantified with the Matrotrophic Index, MI, the dry mass of offspring at birth divided by the dry mass of the egg at fertilization; Reznick et al, 2002;Thompson et al, 2002). The ability to carry multiple broods with varying sizes and to provision those broods throughout embryonic development cause the reproductive strategy of a placentotrophic poeciliid species to be fundamentally different to that of a lecithotrophic species, which provide all resources that it will allocate to the embryo prior to fertilization.…”

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Interpopulation variation in life‐history traits of Poeciliopsis prolifica: implications for the study of placental evolution

2007

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Placental reproduction is widespread across vertebrate taxa, but little is known about its life-history correlates and putative adaptive value. We studied variation in life-history traits in two populations of the placental poeciliid fish Poeciliopsis prolifica to determine whether differences in post-fertilization maternal provisioning to embryos have a genetic basis and how food availability affects reproduction. Life histories were characterized for wild-caught females and for second-generation lab-born females raised under two levels of food availability. We found that the two populations did not differ significantly in the wild for any life-history traits except for the lipid dry weight in females and in embryos at an advanced stage of development. When environmental effects were experimentally controlled, however, populations exhibited significant differences in several traits, including the degree of maternal provisioning to embryos. Food availability significantly affected female size at first parturition, brood size and offspring dry weight at birth. Altogether, these results demonstrate that population differences in maternal provisioning and other life-history traits have a genetic basis and show a plastic response to food availability. We infer that phenotypic plasticity may mask population differences in the field. In addition, when comparing life-history patterns in these two populations with known patterns in placental and non-placental poeciliids, our results support the hypotheses that placentation is an adaptive reproductive strategy under high-resource conditions but that it may represent a cost under low-food conditions. Finally, our results highlight that age at maturity and reproductive allotment may be key life-history traits accompanying placental evolution.

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“…Squamates provide an excellent model to study the evolution of viviparity because viviparity has evolved frequently in squamates (Shine and Bull, 1979;Blackburn, 1982Blackburn, , 1985 and because they exhibit a range of reproductive modes from oviparity to simple (Weekes, 1935) and complex placentation (Flemming and Branch, 2001; Thompson et al, 2002). The evolutionary transition to viviparity requires the retention of the embryo within the uterus for longer and longer periods of time (Shine and Bull, 1979), which in turn requires more sophisticated mechanisms for gas and water exchange and nutrient transport to occur than the eggshell had offered, hence the evolution of the placenta.…”

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Cyto‐epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: A new placental morphotype

Adams

Biazik

Thompson

et al. 2005

Journal of Morphology

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114

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The structural features of the uterine epithelium of the chorioallantoic placenta and omphalloplacenta in the viviparous Australian skink, Pseudemoia entrecasteauxii, were investigated using SEM and TEM techniques. In particular, the structural characteristics that would allow interpretation of function were analyzed, particularly those of gas exchange in the chorioallantoic placenta and histotrophy in the omphaloplacenta. Pseudemoia entrecasteauxii has a complex placenta consisting of a placentome, paraplacentome, and omphaloplacenta. The paraplacentome has a well-vascularized lamina propria in which projecting uterine capillaries displace the overlying uterine epithelial cells, reducing them to attenuated cytoplasmic extensions. Associated cell nuclei and organelles are lost from this region, to provide a capillary lumen to uterine lumen barrier of 0.5-1.0 microm. Hence, the paraplacentome is likely a prominent site for gaseous exchange via simple diffusion. The omphaloplacenta has a similar cytology to that of the placentome, but the uterine epithelial cells are hypertrophied and the apical plasma membrane actively secretes vesicles into the uterine lumen. The omphaloplacenta shows features that are associated with histotrophic transport of nutrients via vesicle secretion, very similar to that of lipid apocrine secretion. The placentome consists of cuboidal cells in the uterine epithelium, with large centrally located nuclei overlying the well-vascularized lamina propria. Although the placentome has a similar cytological structure to that of the omphaloplacenta, granules or active vesicle secretion were not observed. Thus, the placentome may be associated with histotrophy, but not via apocrine secretion. Squamate placentation is epitheliochorial; however, we propose a new term be used to describe the type of placentation in P. entrecasteauxii: "cyto-epitheliochorial," because of the extreme attenuation of uterine epithelial cells of the paraplacentome.

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Evolution of viviparity: what can Australian lizards tell us?

Cited by 43 publications

References 56 publications

Claudin‐5 is Restricted to the Tight Junction Region of Uterine Epithelial Cells in the Uterus of Pregnant/Gravid Squamate Reptiles

Claudin‐5 is Restricted to the Tight Junction Region of Uterine Epithelial Cells in the Uterus of Pregnant/Gravid Squamate Reptiles

Interpopulation variation in life‐history traits of Poeciliopsis prolifica: implications for the study of placental evolution

Cyto‐epitheliochorial placenta of the viviparous lizard Pseudemoia entrecasteauxii: A new placental morphotype

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