Date of Degree

9-2019

Document Type

Dissertation

Degree Name

Ph.D.

Program

Biology

Advisor

Anthony B. Wilson

Committee Members

Jennifer Basil

David Lahti

Nicholas Santangelo

Hope Klug

Subject Categories

Behavior and Ethology | Ecology and Evolutionary Biology | Evolution

Keywords

fish, evolution, parental care, mating behavior, reproductive complexity

Abstract

How does reproductive complexity evolve? In this dissertation, I investigate the evolution of parental investment and mating behavior, using both macro- and microevolutionary lenses. I use fishes, the most diverse group of vertebrates, comprising over 30,000 species, as a model to study the evolution of these traits.

In Chapter 1, I introduce the evolution of parental behaviors in fishes. I present a systematic review of parental care for 294 families (close to 60%) of bony fish and show that male-only care is the predominant form of care in this group. I summarize current theories on parental care, emphasizing external fertilization, certainty of paternity, and territoriality as important factors in the evolution of male care, and internal fertilization as an important precursor to the evolution of female care. I review the social, neural, and physiological mechanisms underlying care behaviors. Finally, I highlight the cichlid model as a remarkably useful system in which to study both the proximate and ultimate causes of parental care.

In Chapter 2, I explore the evolution of parental care and the prevalence of male-only care in bony fishes. Using the most complete phylogeny of bony fishes to date, I show that the opportunity for external fertilization in aquatic environments is a key driver of male parental care in this group. By moving the control of reproduction outside the female reproductive tract, external fertilization increases male confidence in paternity. Paternal care has evolved over 30 times independently in fish and is found only in pair-spawning species, where parentage confidence is high. I demonstrate that females must trade off care against other forms of reproductive investment, while males are not similarly constrained, creating conditions under which both the costs and benefits of care favor paternal investment.

In Chapter 3, I investigate the evolution of biparental care in Cichlidae. I show that evolutionary transitions between biparental and maternal care have occurred frequently, highlighting the evolutionary lability of care in this group. I demonstrate that biparental care is associated with substrate guarding, suggesting that males participate in care when they can benefit from the multiple mating opportunities associated with guarding. Consistent with my findings in Chapter 2, I show that females must trade off care against the number of eggs produced, but that male participation in biparental care can help to offset the costs of female reproduction, allowing for larger clutches. Joint parental care is also associated with extended care duration, suggesting that both parents care when offspring longer periods of care.

Chapters 4 and 5 focus on the evolution of reproductive complexity in the male pregnant pipefish, Syngnathus fuscus. In Chapter 4, I quantify maternal and paternal investment in offspring and test whether relative parental investment predicts intensified sexual selection on females in this group. By weighing newly fertilized and mature embryos, I show, contrary to my predictions, that female care exceeds that of males in this species. I also demonstrate that despite a moderately complex brood pouch, male pregnancy in S. fuscus does not include active provisioning to embryos. Comparison to other pipefish species shows that S. fuscus eggs are on the smallest end of the spectrum, suggesting that this species employs the “quantity over quality” approach, producing many small offspring.

In Chapter 5, I show that Syngnathus fuscus males, despite having some of the highest brood sizes of any pipefish species, consistently mate monogamously across the season. I use molecular markers to reconstruct the number of mothers contributing to the broods of field-caught males, and find that multiple mating among males is rare and occurs only towards the end of the breeding season. I suggest that sex ratio dynamics may influence male monogamy. I also propose that sexual size dimorphism may be responsible for the mating patterns in S. fuscus, as sampled females are larger than males and can fill an entire brood pouch of a male throughout most of the season.

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