Evolutionary ecology of placentation in livebearing fish

I am studying the evolution of the placenta and superfetation in the livebearing fish family Poeciliidae. I study different aspects of these reproductive life history traits, each corresponding to different hypotheses about their evolution.

For an overview of these hypotheses, kindly refer to:

Pollux BJA, Pires MN, Banet AI & Reznick DN (2009) The evolution of placentas in the fish family Poeciliidae - An empirical study of macroevolution. Annu. Rev. Ecol. Evol. Syst. 40:271-289.

Pires MN, Banet AI, Pollux BJA & Reznick DN (2011) Variation and evolution of reproductive strategies. In: J Evans, A Pilastro & I Schlupp (eds), Ecology and Evolution of Poeciliid Fishes. The University of Chicago Press, Chicago, pp.28-37. ISBN-13: 978-0-226-22274-5

The Locomotory Performance Hypothesis

Livebearing is a reproductive strategy that confers both costs and benefits to females. One important cost is a reduction in locomotory performance of the mother during her pregnancy. This can detrimentally influence her feeding efficacy and her ability to avoid predation. Some livebearing organisms have evolved reproductive life-history adaptations that help minimize these locomotory costs.

My PhD students and I are currently adopting a comparative biomechanical (macroevolutionary) approach to test this hypothesis by studying the costs of pregnancy on locomotory performance between closely related livebearing species that either have or lack a placenta and species that either have or lack superfetation. The family Poeciliidae offers a unique opportunity to test this, because both reproductive life history strategies evolved multiple times.

MSc-subjects are:

- Swimming performance in pregnant livebearing fish

- Pregnant fish swimming project

To study why the fish placenta evolved, I propose a more complex microevolutionary approach in which I will link ecological conditions to the biomechanics of swimming performance during pregnancy in an attempt to unravel the potentially adaptive advantages of environmentally induced variation in placentation among natural fish populations in Costa Rica (grant proposal submitted).
With this latter project I aim to provide the first mechanistic explanation for why the placenta evolved. I further plan to establish the fish placenta as a model system for the rapid adaptive evolution of complexity at ecological time-scales.


Photo A
Photo B
Photo C
Photo D

A. seine nets and B. underwater visual census. Main predators of poeciliid species in Costa Rica: C. Eleotris picta (left) and Gobiomorus maculatus (right). D. A captured G. maculatus with a Poeciliopsis turrubarensis in its mouth. (Field work, March-April 2013).

Viviparity-Driven Conflict hypothesis

The evolution of the placenta from a non-placental lecithotrophic ancestor causes a shift of maternal investment from pre- to post-fertilization, creating a venue for parent-offspring conflicts during pregnancy. Theory predicts that the rise of these conflicts should drive a shift from a reliance on pre-copulatory female mate choice to polyandry in conjunction with post-zygotic mechanisms of sexual selection. This hypothesis has not yet been empirically tested. Together with David Reznick, Rob Meredith and Mark Springer, I applied comparative methods to examine potential conflict-driven shifts in sexual selection associated with the evolution of the placenta in the livebearing fish family Poeciliidae. We exploited a unique quality of this family, which is to have evolved placentas at least eight times while retaining close relatives that lack placentas. We have shown that the evolution of post-zygotic maternal provisioning by means of a placenta is associated with the evolutionary loss of bright coloration, courtship behavior and exaggerated ornamental display traits in males. Furthermore, we’ve found that males evolve smaller bodies and longer genitalia, which facilitates sneak or coercive mating and, hence, circumvents female choice. Our results, recently published in Nature, demonstrate that the emergence of prenatal conflict during the evolution of the placenta results in strong directional sexual selection towards a suite of specific phenotypic and behavioral male traits that limit female mate choice prior to copulation.

Pollux BJA, Meredith R, Springer MS & Reznick DN (2014 ) Evolution of the placenta drives a shift in sexual selection in livebearing fish. Nature (2014).

Link: Citizens_Science_Project_Poeciliidae

The Resource Allocation Hypothesis

I found that livebearing fishes with extensive post-fertilization maternal provisioning (placentotrophy), which rely on a continuous supply of resources to nourish their developing offspring (‘Income breeding strategy), display an asynchrony in the adjustment of offspring traits in response to changes in food availability. This asynchrony is not observed in livebearing species with pre-fertilization maternal provisioning (lecithotrophy) that finance reproduction with stored lipid reserves (‘Capital breeding strategy’). The asynchrony limits the ability of placental species to attain an optimal fitness in fluctuating conditions. I’ve therefore argued that the placenta most likely evolved in stable, high-resource environments.

Pollux BJA & Reznick DN (2011) Matrotrophy limits a female’s ability to adaptively adjust offspring size and fecundity in fluctuating environments. Functional Ecology, 25, 747-756.

Pollux BJA & Reznick DN (in prep) The adaptiveness of maternal effects in livebearing fish depends on the mode of maternal provisioning.

Collaborations


This research is performed in close (and pleasant) collaboration with:

- Prof. Dr. D.N. Reznick (UC Riverside, USA)

- Prof. Dr. M.S. Springer (UC Riverside, USA)

- Prof. Dr. T. Garland Jr. (UC Riverside, USA)

- Dr. C. Oufiero (Towson University, USA)

- Dr. A.I. Banet (University of British Colombia, USA)

- Dr. R. Meredith (Montclair State University, USA)

- Mr. A. Furness (UC Riverside, USA)

- Dr. M. Pires (Saddleback Community College, USA)

- Prof. Dr. Ir. J.L. van Leeuwen (Wageningen Universiteit, the Netherlands)

- Dr. MJM Lankheet (Wageningen Universiteit, the Netherlands)


Funding


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