Abstract
Many of our theories for the generation and maintenance of diversity in nature depend on the existence of specialist biotic interactions which, in host–pathogen systems, also shape cross-species disease emergence. As such, niche breadth evolution, especially in host–parasite systems, remains a central focus in ecology and evolution. The predominant explanation for the existence of specialization in the literature is that niche breadth is constrained by trade-offs, such that a generalist is less fit on any particular environment than a given specialist. This trade-off theory has been used to predict niche breadth (co)evolution in both population genetics and eco-evolutionary models, with the different modelling methods providing separate, complementary insights. However, trade-offs may be far from universal, so population genetics theory has also proposed alternate mechanisms for costly generalism, including mutation accumulation. However, these mechanisms have yet to be integrated into eco-evolutionary models in order to understand how the mechanism of costly generalism alters the biological and ecological circumstances predicted to maintain specialism. In this review, we outline how population genetics and eco-evolutionary models based on trade-offs have provided insights for parasite niche breadth evolution and argue that the population genetics-derived mutation accumulation theory needs to be better integrated into eco-evolutionary theory.
Highlights
Why specialists exist in the face of broad-niched generalists remains a central question for both ecology and evolution
Both population genetics and eco-evolutionary theory have important insights on the topic, but these have not yet been well integrated to produce a unifying theory of how both genetic and ecological processes might interact with pathogen biology to shape niche breadth evolution
We argue that further theoretical work is needed to unify these perspectives to predict how niche breadth evolves and how various ecological conditions may bias selection towards generalism or specialism
Summary
Why specialists exist in the face of broad-niched generalists remains a central question for both ecology and evolution. There has been considerable interest in the importance of niche breadth evolution in host–pathogen interactions as these systems may be important drivers of diversity [10,11] and are relevant for multi-host disease transmission and zoonosis [12] For these reasons, the study of pathogen niche breadth (box 1) evolution has flourished in several different subfields including evolutionary genetics, epidemiology and ecology [12,13,14,15]. These subfields’ broad perspectives towards infectious disease evolution differ in several key ways and are not often well integrated, especially across intra- and inter-host scales [16,17] Both population genetics and eco-evolutionary theory have important insights for why generalists are not ubiquitous, but these perspectives have not been well combined for a unified understanding of viral niche breadth evolution [18,19,20,21,22,23], though see [24]. We aim to summarize some of the fundamental assumptions of viral eco-evolutionary and population genetics theory, outline their insights on niche breadth evolution and highlight gaps where these perspectives’ different insights should be united to understand niche breadth dynamics in broader ecological and evolutionary contexts
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