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. 2024 May 30;16(6):evae112. doi: 10.1093/gbe/evae112

Endosymbioses Have Shaped the Evolution of Biological Diversity and Complexity Time and Time Again

Gordon M Bennett 1,2,✉, Younghwan Kwak 3,4, Reo Maynard 5
Editor: Adam Eyre-Walker
PMCID: PMC11154151  PMID: 38813885

Abstract

Life on Earth comprises prokaryotes and a broad assemblage of endosymbioses. The pages of Molecular Biology and Evolution and Genome Biology and Evolution have provided an essential window into how these endosymbiotic interactions have evolved and shaped biological diversity. Here, we provide a current perspective on this knowledge by drawing on decades of revelatory research published in Molecular Biology and Evolution and Genome Biology and Evolution, and insights from the field at large. The accumulated work illustrates how endosymbioses provide hosts with novel phenotypes that allow them to transition between adaptive landscapes to access environmental resources. Such endosymbiotic relationships have shaped and reshaped life on Earth. The early serial establishment of mitochondria and chloroplasts through endosymbioses permitted massive upscaling of cellular energetics, multicellularity, and terrestrial planetary greening. These endosymbioses are also the foundation upon which all later ones are built, including everything from land–plant endosymbioses with fungi and bacteria to nutritional endosymbioses found in invertebrate animals. Common evolutionary mechanisms have shaped this broad range of interactions. Endosymbionts generally experience adaptive and stochastic genome streamlining, the extent of which depends on several key factors (e.g. mode of transmission). Hosts, in contrast, adapt complex mechanisms of resource exchange, cellular integration and regulation, and genetic support mechanisms to prop up degraded symbionts. However, there are significant differences between endosymbiotic interactions not only in how partners have evolved with each other but also in the scope of their influence on biological diversity. These differences are important considerations for predicting how endosymbioses will persist and adapt to a changing planet.

Keywords: endosymbiosis, prokaryotes, eukaryotes, biodiversity, genome evolution, coevolution

Significance.

Understanding how endosymbiotic interactions have coevolved and shaped life on Earth is critical to developing comprehensive theories and predictions in biology. In this perspective, we compare and contrast how major endosymbioses—starting with eukaryogenesis—have influenced biodiversity and the mechanisms that underlie their evolution. We reflect on how significant differences between categories of endosymbioses should influence our theories and predictions about their persistence in nature.

This Perspective is part of a series of articles celebrating 40 years since Molecular Biology and Evolution was founded. It is accompanied by virtual issues on this topic published by Genome Biology and Evolution and Molecular Biology and Evolution, which can be found at our 40th anniversary website.

Introduction

The evolution of all life—from prokaryotes to complex multicellular eukaryotes—has been shaped by symbiotic interactions with the immense microbial diversity that exists on the Earth (McFall-Ngai et al. 2013). Such interactions generally range from antagonistic to beneficial, placing distinctive evolutionary pressures on the interacting partners (Lynch and Hsiao 2019; Drew et al. 2021). In recent years, beneficial symbioses—including facultative and obligate interactions—have become much better understood as important drivers of biological complexity and diversity (Archibald 2014; Douglas 2014; McFall-Ngai 2015; Chomicki et al. 2019; Perreau and Moran 2022). These interactions are diverse in terms of the phylogenetic array of hosts and microbes involved, the specific services that each provides, and the evolutionary mechanisms employed to sustain them. While such beneficial symbioses are diffuse among biological life, endosymbiotic interactions—microbes living inside the cells of a host—are among some of the most ancient and complex biological interactions known (Archibald 2015a). They generally arise when unexploited resources are available but out of reach for potential hosts (Moran 2007). By bridging distant peaks between adaptive landscapes, endosymbionts provide novel phenotypes to their hosts that unlock environmental resources (Fig. 1; Lynch and Hsiao 2019). As a result, endosymbionts are often removed from the open environment and become wholly dependent on their hosts (Bennett and Moran 2015; Drew et al. 2021). Thus, endosymbioses are paragons of coevolution. They entail the complex evolution of integrated genomes, host tissues and organs, novel host cells and cell structures, and mechanisms of resource exchange and communication between the domains of life (Keeling 2013; Martin et al. 2015; Wilson and Duncan 2015).

Fig. 1.

Fig. 1.

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Simplified summary of the major endosymbiotic events that have led to significant leaps in the biological diversity and complexity of life. Endosymbionts provide novel phenotypes to their hosts permitting them to leap between adaptive landscapes with new trait axes and peaks. Except for the establishment of mitochondria during eukaryogenesis, all other endosymbioses are built on the more ancient ones that preceded them. Arrows track the evolutionary progression of these interactions. Peaks and labels illustrate some of the major endosymbiotic events.

Over evolutionary time, endosymbioses have become ecologically pervasive, playing integral roles in shaping—and reshaping again and again—Earth's biological diversity. One could summarize life on our planet as comprising just the prokaryotes and a broad union of organisms derived from endosymbiotic interactions (i.e. anything with mitochondria, plastids, and beyond; Yutin et al. 2008; Martin et al. 2015; Archibald 2015a; McCutcheon et al. 2019). As such, there is an intrinsic and even urgent need to understand the biology and ecology of these interactions. This knowledge is key to discerning the main origins and drivers of biological diversity, as well as to clarifying even our most basic biological and evolutionary theories. Pursuing such grand research goals requires the application of evolutionary principles. This framework elevates questions of “how endosymbioses function” to “why they function,” “where they came from,” and “why they even exist and persist in nature.” It further provides a predictive framework to project our understanding well past our contemporary moment in the evolution of life on Earth.

Building an evolutionary framework into endosymbiosis research necessitates developing a baseline understanding of the diversity, origins, and evolutionary processes underlying these interactions. Over the past 40 years, researchers publishing in the journals, Molecular Biology and Evolution (MBE), and later Genome Biology and Evolution (GBE), have tackled these questions and greatly expanded our knowledge of endosymbioses. What we have learned is profound and voluminous. We take readers through this literature, tackling two basic questions: How have endosymbioses shaped life? And how do endosymbioses evolve?

A Primer on How Endosymbioses Shaped Biological Diversity

With ever more sophisticated molecular tools and technologies, researchers publishing in MBE and GBE have traced the evolution of endosymbioses up and down the tree of life. Early phylogenetic approaches permitted the identification of endosymbiotic partners for many systems and the development of hypotheses about the origin and evolutionary processes shaping these interactions (Moran 1996; Peek et al. 1998; Spaulding and von Dohlen 1998; Pisani et al. 2007). But the greatest accelerant of our understanding of endosymbioses—particularly since few endosymbiotic microbes can be cultured—is the advent of next-generation molecular sequencing (McFall-Ngai 2015). These technologies cheaply expanded the ability to collect complete molecular information for all symbiotic partners (genomes, transcriptomes, proteomes, epigenomes, etc.) across populations, species, and groups (Brown et al. 2015; Chong et al. 2019; Shinzato et al. 2021; Sun et al. 2021; Gould et al. 2022). Research employing these approaches has yielded novel and refined theories of how endosymbioses function and evolve (e.g. McCutcheon and Moran 2010; Sloan et al. 2014; Shapiro et al. 2016; Yang et al. 2020; Ip et al. 2021). Along the way, we have learned that endosymbionts appear to come from almost everywhere and do almost everything. They provide an array of metabolic and physiological services to their hosts, including the exponential upscaling of cellular energy and the bridging of nutritional deficits on land and in the sea (Lane and Martin 2010; Hansen and Moran 2014; Sogin et al. 2021). From eukaryogenesis to the ability of insects to feed on plants, endosymbiosis has been a perpetual driver of biological complexity and diversity (Fig. 1; Archibald 2014; Mills et al. 2022).

The Original Endosymbioses

The first known endosymbiosis of major biological significance occurred ~1.8 billion years ago when Asgard archaean formed an obligate endosymbiotic relationship with an alphaproteobacterium (Sagan 1967; Fitzpatrick et al. 2006; Pisani et al. 2007; Yutin et al. 2008; Williams et al. 2013; Raval et al. 2023). This relationship gave rise to the mitochondria (also mitosomes and hydrogenosomes) and eukaryotes writ large. The precise origins and steps in the coevolutionary integration of the endosymbiotic interaction have been long debated (Thiergart et al. 2012; Williams and Embley 2014; Geiger et al. 2023). (Note: 1.8 billion years of Earth's history is an immense amount of time and space for evolution to scramble its tracks—a common theme in endosymbiosis research.) Nevertheless, recent theory suggests that mitochondria arose in anaerobic conditions through the dependence of methanogenic archaea on H2 provided by an alphaproteobacterial ancestor (Martin and Müller 1998; Mills et al. 2022). The permanent establishment of this alphaproteobacterium into the mitochondria greatly expanded the cellular energy budgets of single-celled and multicellular eukaryotes, further assuming roles in cell cycle regulation, signaling, apoptosis, etc. (Gray et al. 1999; McBride et al. 2006; Roger et al. 2017). The benefit of abundant and localized energy vis-à-vis the mitochondria was a necessary preadaptation for establishing all other endosymbioses that have followed. The mitochondria, by transferring genes to the nuclear genome, also provided genetic toolkits for integrating and sustaining later endosymbioses in more complex hosts (e.g. nutritional endosymbioses in some insects; reviewed by Mao et al. 2018).

Relatively soon after eukaryogenesis (∼1.5 billion years ago), an ancestor to the Archaeplastida (algae and plants) established another significant endosymbiosis with a cyanobacterium (Yoon et al. 2004; Rogozin et al. 2009; Keeling 2013). This relationship led to the primary establishment and evolution of chloroplasts, eukaryotic photosynthesis, massive increases in global primary productivity, and the literal greening of Earth (Moreira et al. 2000; McFadden 2001). Mitochondria were a necessary partner for this event. It provided the fundamental bioenergetic framework to leverage solar energy and the protection of chloroplasts during cellular stress conditions and in the darkness of night (Hoefnagel et al. 1998; Lane and Martin 2010; Mills et al. 2022). In return, the chloroplast endosymbiont provided a ready food source and metabolic support to its mitochondrial partner (e.g. sugars and oxygen; Raghavendra and Padmasree 2003; Oikawa et al. 2021). As a result, some mitochondrial and chloroplast metabolic activities are linked and coregulated by their hosts (Zhang and Glaser 2002; Zhao et al. 2020; He et al. 2023). Some of their essential functions are even supported by the same dual-targeted genes (e.g. essential t-RNA synthesis; Peeters and Small 2001; Carrie et al. 2009; Yogev and Pines 2011). Thus, mitochondria and chloroplasts are, perhaps, the first dual endosymbiosis—a relatively common feature of later endosymbioses of plants and invertebrate animals.

The ability to photosynthesize is such an important adaptive eukaryotic trait that ancestrally nonphototrophic eukaryotes (ancestors to euglenids, apicomplexans, cryptomonads, etc.) have repeatedly stolen the ability (Yoon et al. 2005; Baurain et al. 2010; Dagan et al. 2013; Keeling 2013). Over evolutionary time, and through the process of secondary endosymbiosis, nonphotosynthetic eukaryotic hosts have intracellularly acquired archaeplastid endosymbionts many times and sometimes repeatedly (e.g. tertiary endosymbiosis; Douglas 1998; Keeling 2013). However, the arrangement for the interned photosynthetic eukaryote is less than ideal. The secondary host essentially dissolves the archaeplastid and absorbs necessary genes into its genome to sustain their stolen plastid (Archibald 2015b; Ponce-Toledo et al. 2019). Endosymbioses derived from secondary, tertiary, etc. origins have led to key biological diversity with Earth-changing outcomes (Dorrell and Howe 2015). For example, Symbiodinium dinoflagellates, the product of a red algal secondary endosymbiosis, are themselves endosymbionts of a wide range of marine invertebrates (jellyfish, anemones, nudibranchs, etc.; LaJeunesse et al. 2018; Liu et al. 2018). Notably, Symbiodinium in corals enabled the massive diversification of marine reef systems, which are among the most diverse, important, and threatened ecosystems on the planet (Plaisance et al. 2011; Levin et al. 2016).

The Later Endosymbioses That Shaped Plant and Animal Diversity

Beyond the serial establishment of mitochondria powerhouses and chloroplast primary productivity, disparate eukaryotic lineages have continued acquiring additional endosymbionts. These “later” endosymbioses provided key adaptive advantages to their hosts that generally include novel metabolisms and enhanced access to environmental resources (Moran 2007; Archibald 2014). They have occurred in everything from single-celled eukaryotes (e.g. Paulinella; Marin et al. 2005; Nowack et al. 2008, 2011) to more biologically complex plants and invertebrate animals (e.g. Fabaceae leguminous plants, some marine deep-sea vent invertebrate animals, and hemipteran plant-feeding insects; Sloan et al. 2014; Manzano-Marín et al. 2015; Warshan et al. 2018; Ip et al. 2021). The importance of these endosymbioses in shaping biodiversity is now well in view.

The diversity and success of land plants are attributable, in part, to endosymbiotic interactions with arbuscular mycorrhizae (AM; Parniske 2008; Bonfante and Genre 2010) and nitrogen-fixing cyanobacteria and rhizobia bacteria (Kiers et al. 2003; Warshan et al. 2018). Up to 80% of land plant species engage in endosymbiosis with the ancient Glomeromycota AM (Bennett and Groten 2022). By extending plants’ abilities to scavenge essential nutrients from soils (e.g. nitrogen, phosphorous, and minerals; Parniske 2008), endosymbiosis with AM provided a key adaptive advantage for plants in the terrestrial environment. This relationship was also likely an important factor in the early success of land plants as they established on Earth's barren landscapes >450 million years ago (Delaux and Schornack 2021). In contrast, endosymbioses between land plants and bacteria are comparatively restricted, possibly because plant cell structures and physiology limit intracellular invasion by microbes (Geurts et al. 2016; Delaux and Schornack 2021). Nevertheless, endosymbiotic bacteria in plants have contributed to the ecological success and diversification of several important plant groups. Nitrogen-fixing cyanobacterial endosymbioses have independently evolved in a range of hosts that include Gunnera, some liverworts, cycads, and ferns (Rikkinen 2017; Warshan et al. 2018; Delaux and Schornack 2021). Similarly, root-nodulating rhizobial endosymbioses have led to the diversification of the ecologically and agriculturally important group of plant orders that includes Fabales, Cucurbitales, and Rosales (Markmann and Parniske 2009).

Invertebrate animals have been particularly successful at establishing additional endosymbioses. In an evolutionary framework, these exceedingly diverse interactions permitted hosts to thrive in totally unsuitable environments, often leading to global-scale adaptive species radiations (Moran 2007). For example, a wide diversity of marine invertebrates (e.g. some clam, mussel, and snail species) ally with chemosynthetic bacterial endosymbionts for CO2 fixation into consumable biomass and sugars (Ozawa et al. 2017; Sogin et al. 2020; de Oliveira et al. 2022). These endosymbioses permit their hosts to dominate some of the most extreme and energy-limited environments on Earth, including oceanic sediments and deep-sea thermal vents (Sogin et al. 2021). But this diversity of endosymbioses in invertebrate animals is just the tip of the iceberg.

Far more diverse groups of invertebrate animals, including some nematodes and insects, owe their origins to endosymbioses (Jiggins et al. 2002; Brown et al. 2015; Chong et al. 2019). In particular, insect endosymbioses have received intense attention in recent years. Insects have been dubbed a “fairly land” of endosymbiosis and for good reason (Buchner 1965). These endosymbiotic interactions are responsible for at least 20% of insect species diversity (>1 million species) and underlie their terrestrial dominance (Douglas 2011). Origination events are generally ancient (e.g. tens to hundreds of millions of years old; Bennett and Moran 2013; Patiño-Navarrete et al. 2013) and are too numerous to summarize (e.g. at least ∼50 independent origins in the order Hemiptera, alone; Bennett and Moran 2015; Sudakaran et al. 2017). The principal role of insect endosymbionts is to provide nutrition lacking in host diets (Hansen and Moran 2014). For example, plant sap-feeding insects in the hemipteran order (cicadas, leafhoppers, aphids, whiteflies, etc.) have acquired a diverse array of bacteria to provide essential amino acids lacking in their plant phloem and xylem diets (Sloan and Moran 2013; Santos-Garcia et al. 2014; Mao et al. 2017; Garber et al. 2021). Similar nutritional interactions are known from a broad diversity of insect groups, including ants, cockroaches, and tsetse flies to name just a few (Williams and Wernegreen 2012; Medina Munoz et al. 2017; Kinjo et al. 2018). Insects often take these interactions much further by acquiring multiple endosymbiotic bacteria and fungi that have completely different origins and that make distinct contributions to their endosymbioses (McCutcheon and Moran 2010; Weglarz et al. 2018). They are also actively evolving ever-novel endosymbioses with environmental bacteria (Oakeson et al. 2014), leading to the routine replacement of ancient endosymbionts with younger ones (Sudakaran et al. 2017).

Evolving Biologically Complex Endosymbioses

A major area of interest in evolutionary biology—and Society for Molecular Biology and Evolution (SMBE) journals—is the evolutionary processes that shape the establishment, integration, and long-term persistence of endosymbioses. We have previously described this process as an ever-deepening and spiraling “rabbit hole” (Bennett and Moran 2015). In this framework, endosymbioses are shaped by at least four key factors: (i) the metabolic purpose of the endosymbiosis, (ii) the number of partner endosymbionts involved, (iii) the host’s abilities to transmit and support their endosymbionts across generations, and (iv) the age of the endosymbiosis. The first two factors dictate the minimum genetic repertoire endosymbionts must retain to fulfill their host-dependent functions (e.g. oxidative phosphorylation pathways in mitochondria and nutritional pathways in invertebrate animal endosymbionts; Gray et al. 1999; McCutcheon and Moran 2010). Many symbiotic systems further depend on multiple collaborative endosymbionts to provide single metabolisms (e.g. chloroplast–mitochondrial interactions and dual nutritional endosymbioses in insects; Douglas 2016; Gossett et al. 2023; He et al. 2023). The third factor dictates how strongly host selection and drift are in shaping endosymbiont evolution and the extent to which hosts can support their endosymbionts across generations (Jiggins et al. 2002; Salem et al. 2015; Leftwich et al. 2020; Perreau and Moran 2022; Romero Picazo et al. 2022). The modality in which endosymbionts are acquired (i.e. environmental vs. vertical transmission) generally plays a large role in how these processes unfold over evolutionary time. Finally, as endosymbiotic relationships age, the effects of living in an endosymbiosis become more pronounced on the decreasing cellular and metabolic integrity of endosymbionts (McCutcheon et al. 2019). Hosts, in turn, must continually adapt to sustain their endosymbionts (Mao et al. 2018; Perreau and Moran 2022).

Endosymbiont Evolution: Streamlined for Dysfunction

Perhaps one of the most generalizable outcomes of endosymbiosis is that the genomes and related cellular functionality of endosymbionts are streamlined to fit their ecological and symbiotic requirements. In many cases, this process leads to the extreme reduction of microbial genomes to a mere fraction of those found in their free-living relatives (Khachane et al. 2007; McCutcheon and Moran 2012). However, the obvious effects of genome streamlining are less pronounced in endosymbionts that are horizontally acquired, particularly those with life phases in the open environment (Bright and Bulgheresi 2010; Fisher et al. 2017). For example, while rhizobia bacteria and AM contain genes necessary for their endosymbiotic interactions, they also tend to have large versatile genomes required to cope with complex soil environments (>7 and >150 Mb, respectively; Young et al. 2006; Tisserant et al. 2013).

For vertically transmitted endosymbionts, the evolutionary procession shaping their reduced genomes has been relatively well characterized (Khachane et al. 2007; Wernegreen 2015). Early in the establishment of an endosymbiotic interaction, endosymbiont genomes become adaptively streamlined to lose redundancy with those of their hosts and other endosymbiont partners (Gray et al. 2001; Dale et al. 2003). Genes encoding redundant biosynthetic activities are purged via relaxed selection and eventual excision (Bennett and Moran 2015; Wertheim et al. 2015). This process occurs even in systems with multiple obligate endosymbionts that evolve to perfectly complement each other to meet the needs of their hosts (McCutcheon and Moran 2010; Monnin et al. 2020). However, early on in their establishment when endosymbiont population size and selection are reduced, their genomes can expand with noncoding content that rapidly obliterates redundant and nonessential genes (Koga and Moran 2014; Oakeson et al. 2014). As this early upheaval settles, endosymbiont genomes shrink toward essential integrated metabolisms and functions.

A distinct mode of adaptive genome streamlining occurred in mitochondria, plastids, and the chromatophore of Paulinella. The ancestors of these endosymbionts translocated sizable portions of their genomes to their hosts––a process known as endosymbiotic gene transfer (EGT; Dagan et al. 2013; Ku et al. 2015). The advantages of EGT are thought to lie in host control of gene expression, aiding endosymbiont escape from genetic drift, and economized energetics of protein production and transport (Kelly 2021). The EGT evolutionary process, as well as extreme genome reduction, also occurs in the genomes of primary archaeplastid algal hosts unfortunate enough to become enveloped in secondary endosymbioses with other single-celled eukaryotes (Keeling 2010; Uthanumallian et al. 2022). A significant evolutionary contrast can be made with endosymbionts that are established later in multicellular plant and animal hosts. They generally exhibit little evolutionarily significant EGT. These endosymbionts are rarely in direct contact with germline nuclei and have limited opportunity for heritable EGT to occur (Nikoh et al. 2010).

Finally, as vertically transmitted endosymbioses mature—particularly those found in invertebrate animals—endosymbionts become locked into the endosymbiotic relationship. They experience drastically reduced effective population sizes and strong intergenerational genetic bottlenecks (Moran 1996; Woolfit and Bromham 2003; Vogel and Moran 2013; Hendry et al. 2016). Along with the reduction in their DNA repair mechanisms, drift and the inability to fix errors exaggerate rates of molecular evolution, accumulation of deleterious mutations, and extreme base pair compositional biases (e.g. Douglas et al. 2001; Schelkunov et al. 2015; Waneka et al. 2021). Over time, accumulated mutations cause genes that underlie critical cellular metabolisms and functions to be lost, including the independent ability to regulate genome expression, synthesize membranes and transport metabolites and resources, and even synthesize essential resources required by the host and partner endosymbionts (Kuo et al. 2009; Bennett et al. 2016). These evolutionary processes take their toll on genome size and function, leading to the very smallest known genomes carved out of free-living ancestors (i.e. often just tens to hundreds of kilobases; Gray et al. 2001; Bennett and Moran 2013; Moran and Bennett 2014; Sibbald and Archibald 2020). They also create extreme situations where host lineages and species must adapt to the distinct molecular identities and needs of their endosymbionts through genomic compensation or the acquisition of novel partners (Bennett et al. 2016; Chong et al. 2019; Forsythe et al. 2021; Biot-Pelletier et al. 2023).

Host Evolution: Evolutionary Problem Solvers

Hosts need to overcome a few basic evolutionary challenges in order to sustain and integrate successful endosymbioses with ever-changing partners (Bennett and Moran 2015). These challenges generally include a way to stably exchange essential metabolic and cellular resources, communicate and regulate shared activities, and support ongoing endosymbiont genome degradation. The diverse ways in which hosts meet these challenges depend on the identity of the interacting partners, host anatomy and physiology (e.g. plants vs. animals), and the genetic and genomic constraints of each partner symbiont.

All endosymbioses depend on evolving a means of resource sharing. The sharing of essential metabolites and nutrition is critical to the function and maintenance of endosymbioses (e.g. insect dependence on essential amino acids; Russell et al. 2014; Spinelli and Haigis 2018). The evolution of exchange mechanisms has been accomplished in many ways. The solution depends on the nature of the endosymbiosis and whether endosymbionts retain membrane transport systems and other capabilities in their genomes. Endosymbionts with larger genomes, for example, retain transporters that can handle metabolite exchange (Toft and Fares 2008; Hehenberger et al. 2016). For ancient endosymbionts that no longer encode some or all transporters, hosts contribute them to their membranes and often the entire membrane as well (Price et al. 2011; Duncan et al. 2016; Cunningham and Rutter 2020). But, for unyielding endosymbionts with large independent genomes, such as those acquired from the environment, hosts can either sequester them to elicit and absorb excreted metabolites (e.g. root-nodulating rhizobia; Markmann and Parniske 2009) or simply consume them (e.g. chemosynthetic systems; Sogin et al. 2021).

Due to their tiny genomes, organelles and many endosymbionts also depend on the import of large host nuclear-encoded proteins to perform even their most basic cellular functions. For example, to share protein resources with mitochondria and plastids, eukaryotic hosts have evolved—independently—complex import systems (Tim–Tom and Tic–Toc, respectively; Soll and Schleiff 2004; Wiedemann and Pfanner 2017). In Paulinella—which has in many ways independently replayed chloroplast evolution—protein import re-evolved but the mechanisms appear to have distinct origins, possibly involving the Golgi apparatus (Singer et al. 2017). Similarly, the endosymbionts of invertebrate animals with highly degraded genomes also depend on protein imports, but the mechanisms are currently unclear (Nakabachi et al. 2014; Mao et al. 2018). Due to their many independent origins of endosymbioses in invertebrate animals, the mechanisms responsible for protein import across lineages may very well be cobbled together from distinct genes and cellular machineries.

Host endosymbiont cell–cell regulation and communication are essential for the stable long-term integration of successful endosymbioses. How this has been evolutionarily accomplished across the range of endosymbioses is diverse and complex, and much remains to be understood for many systems. Nevertheless, some mechanisms have been identified in key endosymbioses. In chloroplasts and mitochondria, for example, a process of retrograde signaling modulates host genome activities in response to a range of organelle functions, metabolite presence and abundances, and accumulation of reactive oxygen species (Wang et al. 2020). In plants, both mycorrhizae and rhizobia can use glycan signals to target root cells to establish endosymbiotic association and root nodule formation (Gough and Cullimore 2011). Plant hosts also excrete flavonoid signals that toggle bacterial expression of specific genes important in nodule formation and maintenance (Spaink 2000). After establishment, RNA appears to also play some regulatory roles in nutrient exchange (Xu et al. 2018). In marine endosymbioses between corals and algal dinoflagellates, a complex array of glycans, reactive oxygen species, RNA, and lipids are similarly involved in cell–cell communication and symbiotic regulation (Rosset et al. 2021). For insects, less is currently known about how they regulate and communicate with their diverse nutritional endosymbionts. Some bacterial symbionts with larger genomes maintain complex abilities to monitor and respond to their environments in ways that influence their hosts’ function. These bacterial capabilities include eukaryote targeting effectors and quorum sensing, which are mechanisms for attenuating the host-level fitness costs of harboring endosymbionts (Sanchez-Contreras et al. 2007; Enomoto et al. 2017; Hinzke et al. 2019). However, in the vast majority of ancient insect endosymbioses, these systems have long been lost. An emergent property of some systems is that host-level regulation of endosymbionts may be accomplished through nutrition and metabolite monitoring and exchange. In pea aphids, for example, metabolite transporters sense and regulate the flow of metabolites in response to essential amino acid concentrations (Wilkinson et al. 2007; Duncan et al. 2023).

Finally, maintaining endosymbionts, particularly as they age and degrade into complete dependence, requires the evolution of a multitude of support mechanisms. This process often leads to complex reconfiguration of host genomes. The most extreme is perhaps that of the eukaryotic nuclear genome, which is a core patchwork of archaeal, mitochondrial endosymbiont, and other prokaryotic genes (Ribeiro and Golding 1998; Pisani et al. 2007; Ku et al. 2015; Brueckner and Martin 2020). Accommodating and economizing the early endosymbioses with the mitochondria’s ancestor was accomplished, in part, by absorbing and repurposing parts of its genome through EGT (Martin et al. 1998). A similar process permitted the capture and establishment of chloroplasts (Sibbald and Archibald 2020), as well as the continued acquisition of plastids through secondary endosymbioses (Ponce-Toledo et al. 2018).

For the establishment of later endosymbioses, such as those in insects, the core toolkit is the eukaryotic genome. However, endosymbionts are generally restricted to distinct cells and tissues (e.g. bacteriocytes) that undergo evolutionary modification into tailored support apparatuses (Buchner 1965). The gene expression of these cells is reprogrammed to differentially express thousands of genes responsible for the maintenance and regulation of endosymbionts (e.g. Sloan et al. 2014; Luan et al. 2015). These symbiont-support genes are derived from a range of origins to meet the specific needs of particular endosymbionts. For example, membrane transporters are typically lost from tiny endosymbiont genomes in insects. They often undergo extensive duplication in the host genome and reassignment to the host-endosymbiont interface (Price et al. 2011; Duncan et al. 2016). Another source of aid for later endosymbioses is the preexisting mitochondrial support genes the hosts acquired through ancient EGT. Up to hundreds of these genes are either dual-targeted to mitochondria and nutritional endosymbionts, or they have been duplicated and completely reassigned to support only the latter (Mao et al. 2018). Occasionally, however, the host genome alone cannot close gaps in the metabolic and cellular functions of their endosymbionts. When no other mechanisms are available, hosts resort to acquiring genes through horizontal gene transfer from other infecting bacteria (Sloan et al. 2014; Bublitz et al. 2019). They may also acquire additional symbionts along with their entire genomes (Deng et al. 2023). In essence, hosts pull every evolutionary trick they can to meet the needs of their ever-degrading endosymbionts.

Conclusion

The fields of molecular evolution—and SMBE journals—have tracked decades of scientific discoveries that have revealed the origins, evolution, and global impacts of major endosymbiotic events. This knowledge has invited the reevaluation of long-held theories, including even the fundamental definitions of endosymbioses (i.e. organelles derived from endosymbioses vs. all other kinds of endosymbiotic interactions; see Husnik and Keeling 2019). While the classification of endosymbioses is partly a matter of semantics and theory, the evolutionary implications are important for understanding how endosymbiotic events have influenced biological diversity and how their interactions will persist and adapt to a changing planet. Our accumulated knowledge has revealed that there are indeed important categorical distinctions to make between endosymbiotic systems. We conclude by reviewing two of the more significant ones.

The Important Distinctions between Endosymbioses

The first major distinction between endosymbiotic events is their sharply contrasting scales of influence over the evolution of global biodiversity. At the broadest level, the endosymbiotic steps in eukaryogenesis permitted the adaptive radiation of single-celled eukaryotes, multicellularity, and the eventual evolution of plants and animals (Lane and Martin 2010). The early establishment of mitochondria and chloroplasts is also the essential foundation upon which all other endosymbioses are built. While the later endosymbioses that followed are certainly responsible for the global-scale diversification of many organismal groups, they are comparatively narrow in their host associations and are relatively plastic (Chomicki et al. 2019; Cornwallis et al. 2023). Nutritional endosymbioses in invertebrate animals, for example, have evolved repeatedly between a wide range of hosts, microbial partners, and environments (Sudakaran et al. 2017; Sogin et al. 2021). Many independent events have given rise to a wide diversity of host lineages over space and time. In contrast, mitochondria and chloroplasts are each derived from singular events that enabled the evolution and diversification of everything that is not a prokaryote.

The second important distinction between endosymbioses is that the physical and cellular relationships between partners differentially influence their long-term evolution. Mitochondria, which evolved in single-celled hosts, have proliferated along with nearly every eukaryotic cell, including those comprising multicellular organisms. This is not the case for most later nutritional endosymbionts in multicellular hosts. These endosymbionts generally exist only in highly specialized organs and cells restricted from most others including the germline (Fronk and Sachs 2022). In vertically transmitted endosymbioses (e.g. those found in many insects), tissue and cellular restrictions put their endosymbionts in the perilous situation of having little to no control over their reproductive or evolutionary fates. Consequently, the cellular structures and genomes of vertically transmitted endosymbionts are whittled away to eventual extinction or replacement (McCutcheon et al. 2019). For partnerships where endosymbionts are acquired from the environment (e.g. plant–rhizobial and deep-sea animal–chemosynthetic bacterial endosymbioses), the evolutionary consequences of these associations may be comparatively less severe on endosymbiont genomes and their independent cellular capabilities (Young et al. 2006; Sogin et al. 2021).

Taken together, multicellular hosts that established additional endosymbioses long after eukaryogenesis may have the latitude to evolve away from endosymbioses acquire more partners or swap endosymbionts with better ones (Bennett and Moran 2015). They cannot as easily drop their dependence on mitochondria and, to a more limited extent, chloroplasts. These first endosymbionts have ensured their essentiality and near immortality among eukaryotic cells. Thus, it may be predicted that for as long as eukaryotes and photosynthesis persist on Earth, so too will mitochondria and chloroplasts. The same cannot be said for other kinds of endosymbioses.

Acknowledgments

We thank Maggie Sogin and the National Science Foundation Biological Integration Institute INSITE team for helpful discussions on endosymbiosis theory and the biology of specific systems. Heather Stever provided thoughtful reviews and edits on early versions of this work. We also thank the SMBE editors for inviting and considering our manuscript. We also thank Dr. Adam Eyre-Walker. We apologize for any of the important work and authors that we may have missed in our attempt to cover a broad topic.

Contributor Information

Gordon M Bennett, Department of Life and Environmental Sciences, University of California, Merced, CA, USA; National Science Foundation Biological Integration Institute—INSITE, University of California, Merced, CA, USA.

Younghwan Kwak, Department of Life and Environmental Sciences, University of California, Merced, CA, USA; National Science Foundation Biological Integration Institute—INSITE, University of California, Merced, CA, USA.

Reo Maynard, Department of Life and Environmental Sciences, University of California, Merced, CA, USA.

Author Contributions

G.M.B. devised the main conceptual ideas, outlined the structure and story, conducted an extensive MBE literature review, collated outstanding MBE papers, synthesized the information, wrote and revised the majority of the manuscript, and approved the final version for submission. Y.K. contributed to early discussions on manuscript concepts, conducted an extensive GBE literature review, collated outstanding GBE papers, synthesized the information, drafted sections on endosymbiont and host genome evolution, and revised the manuscript. R.M. synthesized and helped collect relevant papers, drafted sections on the origin and later endosymbioses in the initial manuscript, and revised the manuscript.

Funding

This work was supported by the National Science Foundation (NSF-1347116 to G.M.B.) and the Howard Hughes Medical Institute (GT15982 to R.M.).

Data Availability

No new data were produced.

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