Predation as a driver of reproductive isolation - from adaptive divergence to hybrid inviability

Research output: ThesisDoctoral Thesis (compilation)

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Abstract

Natural selection can play an important role in the origin of new species. When reproductive isolation evolves as a result of ecologically-based divergent natural selection, the process is referred to as ecological speciation. In most organisms, sufficient reproductive isolation is considered to be essential for the establishment of new species. However, reproductive isolation typically involves multiple isolating barriers, and we still lack knowledge of how some barriers are affected by the level of ecological divergence and the stage of speciation.

The aim of this thesis is to estimate how a potent source of ecological selection, predation, may drive reproductive isolation. First, I study multiple isolated populations of Bahamas mosquitofish (Gambusia hubbsi), that have adapted to either of two distinct selective regimes depending on the presence or absence of predatory fish. I estimate how the behaviour of mosquitofish has diverged under these contrasting predation regimes, and whether reproductive isolation has evolved to be stronger between populations from different predation regimes. Second, I study the behavioural phenotype of naturally occurring hybrids between roach (Rutilus rutilus) and common bream (Abramis brama), and ask if maladaptive behaviour can underlie increased susceptibility to predation in hybrids.

Through behavioural trials using either wild-caught or laboratory-reared Bahamas mosquitofish, I show that key behavioural traits have diverged between predation regimes, but also highlight that the degree of divergence is often sex specific. I found that low-predation environments may select for foraging traits that are likely beneficial under high resource competition, but this effect was only seen in the female sex. I also show that male, but not female, mating behaviours have diverged between predation regimes, as males adapted to a high-predation regime courted females and attempted to initiate mating more actively in comparison to males originating from low-predation environments. By comparing behavioural traits expressed during within-population and between-population mating trials, I discovered that females were more aggressive towards foreign males and initiated aggression faster towards males from the opposite predation regime. I thus show that ecological adaptation may act to strengthen behavioural isolation between populations in this system.

Furthermore, I show that hybrids produced between parents originating from different predation regimes have the lowest survival rates out of all hybrids and pure-line offspring reared in common-garden conditions. This indicates that ecological divergence can lead to intrinsic hybrid incompatibilities relatively early along the speciation continuum. The hybrid crosses between different predation regimes also showed intermediate fast-start escape-performance abilities when compared to crosses within the same predation regime, indicating that hybrids produced between divergently adapted populations may have lower ecological viability in the high-predation environment. Monitoring of the migration patterns through passive telemetry revealed that roach × bream hybrids show a higher frequency of migratory trips between the stream and lake habitats, a behaviour that exposes them to a higher predation risk. I thus show that predation can reinforce species integrity by selecting against hybrid phenotypes.

In summary, differences in predation risk between populations can lead to stronger reproductive isolation as a by-product of adaptive divergence. Furthermore, several forms of pre- and postzygotic isolation may be important for this process, even at an early stage of speciation. Finally, predation may also play an important role in the later stages of speciation as a reinforcer of species integrity.
Original languageEnglish
QualificationDoctor
Awarding Institution
  • Aquatic Ecology
Supervisors/Advisors
  • Nilsson, Anders, Supervisor
  • Hulthén, Kaj, Assistant supervisor
  • Brönmark, Christer, Assistant supervisor
Award date2021 Dec 3
Place of PublicationLund
Publisher
ISBN (Print)978-91-8039-068-2
ISBN (electronic) 978-91-8039-067-5
Publication statusPublished - 2021

Bibliographical note

Defence details
Date: 2021-12-03
Time: 09:00
Place: The Blue Hall, Ekologihuset, Biologiska institutionen. Join via zoom: https://lu-se.zoom.us/j/62442225271?pwd=Q2MwR3IwaG1xZWVLemREYUdldk5DUT09 passcode: 496711
External reviewer(s)
Name: Qvarnström, Anna
Title: Professor
Affiliation: Uppsala universitet
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Subject classification (UKÄ)

  • Evolutionary Biology

Keywords

  • reproductive isolation
  • ecological speciation
  • predation
  • adaptive radiation
  • evolution
  • behaviour
  • fish

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