scholarly journals Microbiome-mediated plasticity directs host evolution along several distinct time scales

2020 ◽  
Vol 375 (1808) ◽  
pp. 20190589 ◽  
Author(s):  
Oren Kolodny ◽  
Hinrich Schulenburg

Host-associated microbiomes influence their host's fitness in myriad ways and can be viewed as a source of phenotypic plasticity. This plasticity may allow the host to accommodate novel environmental challenges and thus influence the host's evolutionary adaptation. As with other modalities of phenotypic plasticity in phenomena such as the Baldwin effect and genetic assimilation, the microbiome-mediated plasticity may influence host genetic adaptation by facilitating and accelerating it, by slowing it down, or even by preventing it. The dynamics involved are likely more complex than those of previously studied phenomena related to phenotypic plasticity, and involve different processes on each time scale, such as acquired recognition of newly associated microbes by the host's immune system on single- and multiple-generation time scales, or selection on transmission dynamics of microbes between hosts, acting on longer time scales. To date, it is unclear if and how any of these processes shape host evolution. This opinion piece article provides a conceptual framework for considering the processes by which microbiome-mediated plasticity directs host evolution and concludes with suggestions for key experimental tests of the presented ideas. This article is part of the theme issue ‘The role of the microbiome in host evolution’.

2002 ◽  
Vol 8 (4) ◽  
pp. 311-339 ◽  
Author(s):  
Steve Munroe ◽  
Angelo Cangelosi

The Baldwin effect has been explicitly used by Pinker and Bloom as an explanation of the origins of language and the evolution of a language acquisition device. This article presents new simulations of an artificial life model for the evolution of compositional languages. It specifically addresses the role of cultural variation and of learning costs in the Baldwin effect for the evolution of language. Results show that when a high cost is associated with language learning, agents gradually assimilate in their genome some explicit features (e.g., lexical properties) of the specific language they are exposed to. When the structure of the language is allowed to vary through cultural transmission, Baldwinian processes cause, instead, the assimilation of a predisposition to learn, rather than any structural properties associated with a specific language. The analysis of the mechanisms underlying such a predisposition in terms of categorical perception supports Deacon's hypothesis regarding the Baldwinian inheritance of general underlying cognitive capabilities that serve language acquisition. This is in opposition to the thesis that argues for assimilation of structural properties needed for the specification of a full-blown language acquisition device.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190594 ◽  
Author(s):  
Samantha S. Fontaine ◽  
Kevin D. Kohl

Host-associated microbial communities have profound impacts on animal physiological function, especially nutrition and metabolism. The hypothesis of ‘symmorphosis’, which posits that the physiological systems of animals are regulated precisely to meet, but not exceed, their imposed functional demands, has been used to understand the integration of physiological systems across levels of biological organization. Although this idea has been criticized, it is recognized as having important heuristic value, even as a null hypothesis, and may, therefore, be a useful tool in understanding how hosts evolve in response to the function of their microbiota. Here, through a hologenomic lens, we discuss how the idea of symmorphosis may be applied to host-microbe interactions. Specifically, we consider scenarios in which host physiology may have evolved to collaborate with the microbiota to perform important functions, and, on the other hand, situations in which services have been completely outsourced to the microbiota, resulting in relaxed selection on host pathways. Following this theoretical discussion, we finally suggest strategies by which these currently speculative ideas may be explicitly tested to further our understanding of host evolution in response to their associated microbial communities. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190603 ◽  
Author(s):  
Angela E. Douglas

In many animal hosts, microbial symbionts are housed within specialized structures known as symbiotic organs, but the evolutionary origins of these structures have rarely been investigated. Here, I adopt an evolutionary developmental (evo-devo) approach, specifically to apply knowledge of the development of symbiotic organs to gain insights into their evolutionary origins and diversification. In particular, host genetic changes associated with evolution of symbiotic organs can be inferred from studies to identify the host genes that orchestrate the development of symbiotic organs, recognizing that microbial products may also play a key role in triggering the developmental programme in some associations. These studies may also reveal whether higher animal taxonomic groups (order, class, phylum, etc.) possess a common genetic regulatory network for symbiosis that is latent in taxa lacking symbiotic organs, and activated at the origination of symbiosis in different host lineages. In this way, apparent instances of convergent evolution of symbiotic organs may be homologous in terms of a common genetic blueprint for symbiosis. Advances in genetic technologies, including reverse genetic tools and genome editing, will facilitate the application of evo-devo approaches to investigate the evolution of symbiotic organs in animals. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190593 ◽  
Author(s):  
Spencer V. Nyholm

Microorganisms are associated with the eggs of many animals. For some hosts, the egg serves as the ideal environment for the vertical transmission of beneficial symbionts between generations, while some bacteria use the egg to parasitize their hosts. In a number of animal groups, egg microbiomes often perform other essential functions. The eggs of aquatic and some terrestrial animals are especially susceptible to fouling and disease since they are exposed to high densities of microorganisms. To overcome this challenge, some hosts form beneficial associations with microorganisms, directly incorporating microbes and/or microbial products on or in their eggs to inhibit pathogens and biofouling. Other functional roles for egg-associated microbiomes are hypothesized to involve oxygen and nutrient acquisition. Although some egg-associated microbiomes are correlated with increased host fitness and are essential for successful development, the mechanisms that lead to such outcomes are often not well understood. This review article will discuss different functions of egg microbiomes and how these associations have influenced the biology and evolution of animal hosts. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190604 ◽  
Author(s):  
Britt Koskella ◽  
Joy Bergelson

Microorganismal diversity can be explained in large part by selection imposed from both the abiotic and biotic environments, including—in the case of host-associated microbiomes—interactions with eukaryotes. As such, the diversity of host-associated microbiomes can be usefully studied across a variety of scales: within a single host over time, among host genotypes within a population, between populations and among host species. A plethora of recent studies across these scales and across diverse systems are: (i) exemplifying the importance of the host genetics in shaping microbiome composition; (ii) uncovering the role of the microbiome in shaping key host phenotypes; and (iii) highlighting the dynamic nature of the microbiome. They have also raised a critical question: do these complex associations fit within our existing understanding of evolution and coevolution, or do these often intimate and seemingly cross-generational interactions follow novel evolutionary rules from those previously identified? Herein, we describe the known importance of (co)evolution in host–microbiome systems, placing the existing data within extant frameworks that have been developed over decades of study, and ask whether there are unique properties of host–microbiome systems that require a paradigm shift. By examining when and how selection can act on the host and its microbiome as a unit (termed, the holobiont), we find that the existing conceptual framework, which focuses on individuals, as well as interactions among individuals and groups, is generally well suited for understanding (co)evolutionary change in these intimate assemblages. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2020 ◽  
Vol 375 (1808) ◽  
pp. 20190599 ◽  
Author(s):  
Yael Gurevich ◽  
Ohad Lewin-Epstein ◽  
Lilach Hadany

Paternal care, particularly in cases of uncertain paternity, carries significant costs. Extensive research, both theoretical and experimental, has explored the conditions in which paternal care behaviour would be favoured. Common explanations include an adjustment of care with uncertainty in paternity and limited accuracy in parentage assessment. Here, we propose a new explanation that microbes may play a role in the evolution of paternal care among their hosts. Using computational models, we demonstrate that microbes associated with increased paternal care could be favoured by natural selection. We find that microbe-induced paternal care could evolve under wider conditions than suggested by genetic models. Moreover, we show that microbe-induced paternal care is more likely to evolve when considering paternal care interactions that increase microbial transmission, such as feeding and grooming. Our results imply that factors affecting the composition of host microbiome may also alter paternal behaviour. This article is part of the theme issue ‘The role of the microbiome in host evolution’.


2007 ◽  
Vol 13 (1) ◽  
pp. 31-43 ◽  
Author(s):  
Reiji Suzuki ◽  
Takaya Arita

The interaction between evolution and learning called the Baldwin effect is a two-step evolutionary scenario caused by the balances between benefit and cost of learning in general. However, little is known about the dynamic evolution of these balances in complex environments. Our purpose is to give a new insight into the benefit and cost of learning by focusing on the quantitative evolution of phenotypic plasticity under the assumption of epistatic interactions. For this purpose, we have constructed an evolutionary model of quantitative traits by using an extended version of Kauffman's NK fitness landscape. Phenotypic plasticity is introduced into our model; whether each phenotype is plastic or not is genetically defined, and plastic phenotypes can be adjusted by learning. The simulation results clearly show that drastic changes in roles of learning cause three-step evolution through the Baldwin effect and also cause the evolution of genetic robustness against mutations. We also conceptualize four different roles of learning by using a hill-climbing image of a population on a fitness landscape.


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