Major Evolutionary Transitions Research Articles

Olfactory coding in the antennal lobe of the bumble bee Bombus terrestris

Sociality is classified as one of the major transitions in evolution, with the largest number of eusocial species found in the insect order Hymenoptera, including the Apini (honey bees) and the Bombini (bumble bees). Bumble bees and honey bees not only differ in their social organization and foraging strategies, but comparative analyses of their genomes demonstrated that bumble bees have a slightly less diverse family of olfactory receptors than honey bees, suggesting that their olfactory abilities have adapted to different social and/or ecological conditions. However, unfortunately, no precise comparison of olfactory coding has been performed so far between honey bees and bumble bees, and little is known about the rules underlying olfactory coding in the bumble bee brain. In this study, we used in vivo calcium imaging to study olfactory coding of a panel of floral odorants in the antennal lobe of the bumble bee Bombus terrestris. Our results show that odorants induce reproducible neuronal activity in the bumble bee antennal lobe. Each odorant evokes a different glomerular activity pattern revealing this molecule’s chemical structure, i.e. its carbon chain length and functional group. In addition, pairwise similarity among odor representations are conserved in bumble bees and honey bees. This study thus suggests that bumble bees, like honey bees, are equipped to respond to odorants according to their chemical features.

A broadscale analysis of host-symbiont cophylogeny reveals the drivers of phylogenetic congruence.

Symbioses exert substantial biological influence, with great evolutionary and ecological relevance for disease, major evolutionary transitions, and the structure and function of ecological communities. Yet, much remains unknown about the patterns and processes that characterise symbioses. A major unanswered question is the extent to which symbiont phylogenies mirror those of their hosts and if patterns differ for parasites and mutualists. Addressing this question offers fundamental insights into evolutionary processes, such as whether symbionts typically codiverge with their hosts or if diversity is generated via host switches. Here, we perform a meta-analysis of host-symbiont phylogenetic congruence, encompassing 212 host-symbiont cophylogenetic studies that include ~10,000 species. Our analysis supersedes previous qualitative assessments by utilising a quantitative framework. We show that symbiont phylogeny broadly reflects host phylogeny across biodiversity and life-history, demonstrating a general pattern of phylogenetic congruence in host-symbiont interactions. We reveal two key aspects of symbiont life-history that promote closer ties between hosts and symbionts: vertical transmission and mutualism. Mode of symbiosis and mode of transmission are intimately interlinked, but vertical transmission is the dominant factor. Given the pervasiveness of symbioses, these findings provide important insights into the processes responsible for generating and maintaining the Earth's rich biodiversity.

Macroevolution of dimensionless life-history metrics in tetrapods.

Life-history traits represent organisms' strategies to navigate the fitness trade-offs between survival and reproduction. Eric Charnov developed three dimensionless metrics to quantify fundamental life-history trade-offs. Lifetime reproductive effort (LRE), relative reproductive lifespan (RRL) and relative offspring size (ROS), together with body mass can be used to classify life-history strategies across the four major classes of tetrapods: amphibians, reptiles, mammals and birds. First, we investigate how the metrics have evolved in concert with body mass within tetrapod lineages. In most cases, we find evidence for correlated evolution among body mass and the three dimensionless metrics. Second, we compare life-history strategies across the four classes of tetrapods and find that LRE, RRL and ROS delineate a space in which the major tetrapod classes occupy mostly unique subspaces. These distinct combinations of life-history strategies provide us with a framework to understand the impact of major evolutionary transitions in energetics, physiology and ecology.

Eusociality through conflict dissolution.

Eusociality, where largely unreproductive offspring help their mothers reproduce, is a major form of social organization. An increasingly documented feature of eusociality is that mothers induce their offspring to help by means of hormones, pheromones or behavioural displays, with evidence often indicating that offspring help voluntarily. The co-occurrence of maternal influence and offspring voluntary help may be explained by what we call the converted helping hypothesis, whereby maternally manipulated helping subsequently becomes voluntary. Such hypothesis requires that parent-offspring conflict is eventually dissolved—for instance, if the benefit of helping increases sufficiently over evolutionary time. We show that help provided by maternally manipulated offspring can enable the mother to sufficiently increase her fertility to transform parent-offspring conflict into parent-offspring agreement. This conflict-dissolution mechanism requires that helpers alleviate maternal life-history trade-offs, and results in reproductive division of labour, high queen fertility and honest queen signalling suppressing worker reproduction—thus exceptionally recovering diverse features of eusociality. As such trade-off alleviation seemingly holds widely across eusocial taxa, this mechanism offers a potentially general explanation for the origin of eusociality, the prevalence of maternal influence, and the offspring’s willingness to help. Overall, our results explain how a major evolutionary transition can happen from ancestral conflict.

The weird eusociality of polyembryonic parasites.

Some parasitoid wasps possess soldier castes during their parasitic larval stage, but are often neglected from our evolutionary theories explaining caste systems in animal societies. This is primarily due to the polyembryonic origin of their societies. However, recent discoveries of polyembryonic trematodes (i.e. flatworms) possessing soldier castes require us to reconsider this reasoning. I argue we can benefit from including these polyembryonic parasites in eusocial discussions, for polyembryony and parasitism are taxonomically vast and influence the evolution of social behaviours and caste systems in various circumstances. Despite their polyembryony, their social evolution can be explained by theories of eusociality designed for parent–offspring groups, which are the subjects of most social evolution research. Including polyembryonic parasites in these theories follows the trend of major evolutionary transitions theory expanding social evolution research into all levels of biological organization. In addition, these continued discoveries of caste systems in parasites suggest social evolution may be more relevant to parasitology than currently acknowledged.

Genome-wide analyses across Viridiplantae reveal the origin and diversification of small RNA pathway-related genes

Small RNAs play a major role in the post-transcriptional regulation of gene expression in eukaryotes. Despite the evolutionary importance of streptophyte algae, knowledge on small RNAs in this group of green algae is almost non-existent. We used genome and transcriptome data of 34 algal and plant species, and performed genome-wide analyses of small RNA (miRNA & siRNA) biosynthetic and degradation pathways. The results suggest that Viridiplantae started to evolve plant-like miRNA biogenesis and degradation after the divergence of the Mesostigmatophyceae in the streptophyte algae. We identified two major evolutionary transitions in small RNA metabolism in streptophyte algae; during the first transition, the origin of DCL-New, DCL1, AGO1/5/10 and AGO4/6/9 in the last common ancestor of Klebsormidiophyceae and all other streptophytes could be linked to abiotic stress responses and evolution of multicellularity in streptophytes. During the second transition, the evolution of DCL 2,3,4, and AGO 2,3,7 as well as DRB1 in the last common ancestor of Zygnematophyceae and embryophytes, suggests their possible contribution to pathogen defense and antibacterial immunity. Overall, the origin and diversification of DICER and AGO along with several other small RNA pathway-related genes among streptophyte algae suggested progressive adaptations of streptophyte algae during evolution to a subaerial environment.

Quantifying the middle–late Cambrian trilobite diversity pattern in South China

The middle–late Cambrian is a key interval between the Cambrian Explosion and the Great Ordovician Biodiversification Event (GOBE) that marks a major biologic evolutionary transition in the geologic record. Diversity (i.e. richness) patterns in this interval show that macro-biota experienced evolutionary setbacks for the first time. However, relatively little attention has been paid to this interval in previous macroevolutionary studies and very different conclusions about the diversity patterns in coarse time-resolution have been documented. As a dominate group of marine benthic organisms in the Cambrian, trilobites provide insightful information to understand the history of biodiversity in the Cambrian marine ecosystem from the Cambrian Explosion to the GOBE. South China is a region with relatively good preservation of Cambrian fossil materials and sections, and 4 out of 6 Cambrian GSSPs were established in South China. In this paper, we use constrained optimization (CONOP) to correlate 19 sections from South China to reduce the Signor-Lipps effect and integrate the results with high-resolution chronostratigraphic data to evaluate the middle–late Cambrian trilobite diversity pattern in South China. This study, for the first time, constructs a high time-resolution (about 60 kyr) trilobite species-level richness curve with estimated time from Age 4 to the Paibian. A double-peaked species diversification is separated by a minor extinction in Stage 4; this is followed by a gradual decline of species diversity over the entire Wuliuan Age. A radiation of three times increase of species diversity in the Drumian and Guzhangian is exhibited and the diversity remains high for most of the Guzhangian Stage; this is followed by a great extinction at the end of the Guzhangian with around 50% species lost. Detailed comparison with previous composite studies and fossil material from single sections revealed that the Signor-Lipps effect could produce large biases in diversity pattern. In addition, a precise analysis of species evolution features compared with environmental indices provides a perspective about trilobite evolutionary mechanisms associated with environmental changes related to the carbon cycle and biotic competition.

Adaptive landscapes challenge the “lateral-to-sagittal” paradigm for mammalian vertebral evolution

The evolution of mammals from their extinct forerunners, the non-mammalian synapsids, is one of the most iconic locomotor transitions in the vertebrate fossil record. In the limb skeleton, the synapsid-mammal transition is traditionally characterized by a shift from a sprawling limb posture, resembling that of extant reptiles and amphibians, to more adducted limbs, as seen in modern-day mammals. Based on proposed postural similarities between early synapsids and extant reptiles, this change is thought to be accompanied by a shift from ancestral reptile-like lateral bending to mammal-like sagittal bending ofthe vertebral column. To test this "lateral-to-sagittal" evolutionary paradigm, we used combinatorial optimization to produce functionally informed adaptive landscapes and determined the functional trade-offs associated with evolutionary changes in vertebral morphology. We show that the synapsid adaptive landscape is different from both extant reptiles and mammals, casting doubt on the reptilian model for early synapsid axial function, or indeed for the ancestral condition of amniotes more broadly. Further, the synapsid-mammal transition is characterized by not only increasing sagittal bending in theposterior column but also high stiffness and increasing axial twisting in the anterior column. Therefore,we refute the simplistic lateral-to-sagittal hypothesis and instead suggest the synapsid-mammal locomotor transition involved a more complex suite of functional changes linked to increasing regionalization of the backbone. These results highlight the importance of fossil taxa for understanding major evolutionary transitions.

Vertebrate Life, 10th edition

Vertebrate Life, 10th edition

Transposable Elements and Stress in Vertebrates: An Overview.

Since their identification as genomic regulatory elements, Transposable Elements (TEs) were considered, at first, molecular parasites and later as an important source of genetic diversity and regulatory innovations. In vertebrates in particular, TEs have been recognized as playing an important role in major evolutionary transitions and biodiversity. Moreover, in the last decade, a significant number of papers has been published highlighting a correlation between TE activity and exposition to environmental stresses and dietary factors. In this review we present an overview of the impact of TEs in vertebrate genomes, report the silencing mechanisms adopted by host genomes to regulate TE activity, and finally we explore the effects of environmental and dietary factor exposures on TE activity in mammals, which is the most studied group among vertebrates. The studies here reported evidence that several factors can induce changes in the epigenetic status of TEs and silencing mechanisms leading to their activation with consequent effects on the host genome. The study of TE can represent a future challenge for research for developing effective markers able to detect precocious epigenetic changes and prevent human diseases.

Evidence for reduced immune gene diversity and activity during the evolution of termites.

The evolution of biological complexity is associated with the emergence of bespoke immune systems that maintain and protect organism integrity. Unlike the well-studied immune systems of cells and individuals, little is known about the origins of immunity during the transition to eusociality, a major evolutionary transition comparable to the evolution of multicellular organisms from single-celled ancestors. We aimed to tackle this by characterizing the immune gene repertoire of 18 cockroach and termite species, spanning the spectrum of solitary, subsocial and eusocial lifestyles. We find that key transitions in termite sociality are correlated with immune gene family contractions. In cross-species comparisons of immune gene expression, we find evidence for a caste-specific social defence system in termites, which appears to operate at the expense of individual immune protection. Our study indicates that a major transition in organismal complexity may have entailed a fundamental reshaping of the immune system optimized for group over individual defence.

What are the major transitions?

The ‘Major Transitions in Evolution’ (MTE) framework has emerged as the dominant paradigm for understanding the origins of life's hierarchical organization, but it has been criticized on the grounds that it lacks theoretical unity, that is, that the events included in the framework do not constitute a coherent category. I agree with this criticism, and I argue that the best response is to modify the framework so that the events it includes do comprise a coherent category, one whose members share fundamental similarities. Specifically, I recommend defining major transitions as all those, and only those, events and processes that result in the emergence of a new population of evolutionary individuals. Two sorts of change will be required to achieve this. First, events and processes that do not meet this criterion, such as the origins of the genetic code and of human language, should be excluded. Second, events and processes that do meet the criterion, but which have generally been neglected, should be included. These changes would have the dual benefits of making MTEs a philosophically coherent category and of increasing the sample size on which we may infer trends and general principles that may apply to all MTEs.

The late appearance of DNA, the nature of the LUCA and ancestors of the domains of life

It has been firmly observed that replicative DNA polymerases of bacteria, archaea and eukaryotes are not homologous proteins. This lack of homology in the replication apparatus among the domains of life is not only compatible with but would seem to imply the view that the emergence of DNA occurred in the fundamental cellular lineages. In consequence, this diversity of DNA polymerase would go back to the level of ancestors of the domains of life and to the evolutionary time in which the DNA emerged. Therefore, the presumed evolutionary stage linked to the RNA- > DNA transition would have occurred only at the level of ancestors of the main lineages of the tree of life. Thus, the high noise associated with this major evolutionary transition and the impossibility for a cellular stage to generate different fundamental genetically profound traits - such as the different replication apparatuses of bacteria, archaea and eukaryotes - would imply not only that the last universal common ancestor (LUCA) was a progenote but that the ancestors of the domains of life were also at this evolutionary stage. So, I criticize the hypotheses which want, instead, that completely different cells - such as, bacteria and archaea - could have originated from a cellular LUCA.

Non-genetic inheritance: Evolution above the organismal level

The article proposes to further develop the ideas of the Extended Evolutionary Synthesis by including into evolutionary research an analysis of phenomena that occur above the organismal level. We demonstrate that the current Extended Synthesis is focused more on individual traits (genetically or non-genetically inherited) and less on community system traits (synergetic/organizational traits) that characterize transgenerational biological, ecological, social, and cultural systems. In this regard, we will consider various communities that are made up of interacting populations, and for which the individual members can belong to the same or to different species. Examples of communities include biofilms, ant colonies, symbiotic associations resulting in holobiont formation, and human societies. The proposed model of evolution at the level of communities revises classic theorizing on the major transitions in evolution by analyzing the interplay between community/social traits and individual traits, and how this brings forth ideas of top-down regulations of bottom-up evolutionary processes (collaboration of downward and upward causation). The work demonstrates that such interplay also includes reticulate interactions and reticulate causation. In this regard, we exemplify how community systems provide various non-genetic ‘scaffoldings’, ‘constraints’, and ‘affordances’ for individual and sociocultural evolutionary development. Such research complements prevailing models that focus on the vertical transmission of heritable information, from parent to offspring, with research that instead focusses on horizontal, oblique and even reverse information transmission, going from offspring to parent. We call this reversed information transfer the ‘offspring effect’ to contrast it from the ‘parental effect’. We argue that the proposed approach to inheritance is effective for modelling cumulative and distributed developmental process and for explaining the biological origins and evolution of language.

Pollen feeding in Heliconius butterflies: the singular evolution of an adaptive suite.

Major evolutionary transitions can be triggered by behavioural novelty, and are often associated with 'adaptive suites', which involve shifts in multiple co-adapted traits subject to complex interactions. Heliconius butterflies represent one such example, actively feeding on pollen, a behaviour unique among butterflies. Pollen feeding permits a prolonged reproductive lifespan, and co-occurs with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits that are absent in closely related, non-pollen-feeding genera. As a highly tractable system, supported by considerable ecological and genomic data, Heliconius are an excellent model for investigating how behavioural innovation can trigger a cascade of adaptive shifts in multiple diverse, but interrelated, traits. Here, we synthesize current knowledge of pollen feeding in Heliconius, and explore potential interactions between associated, putatively adaptive, traits. Currently, no physiological, morphological or molecular innovation has been explicitly linked to the origin of pollen feeding, and several hypothesized links between different aspects of Heliconius biology remain poorly tested. However, resolving these uncertainties will contribute to our understanding of how behavioural innovations evolve and subsequently alter the evolutionary trajectories of diverse traits impacting resource acquisition, life history, senescence and cognition.

The rise of languaging

In this paper, we turn to languaging, defined here as activity in which wordings play a part. On such a view, while activity is paramount, people also orient to acts of vocalization as wordings. These physical wordings can be used as tools that shape attending, with recourse to neither mental representations nor symbols that store and transmit information. The view is consistent with macroevolutionary continuity and will be used to challenge appeal to a major evolutionary transition to ‘language’. On the languaging view, like many modern social primates, hominins have long undertaken encultured activities. Infants, human and nonhuman, act epistemically and, by so doing, align skills with objects to practice. They develop a ‘stance’ to pragmatic, goal-directed action. In human ontogenesis, we argue, both epistemic action and the stance-taking are extended by vocalizing. Caregiver-infant coordination enables vocalizing to be integrated with acting, attending, perceiving and managing one’s attention. Infants also self-entrain vocalizing through ‘babble’. Once the developmental threads unite, social reaching (Bates, 1976) favors a special stance to articulatory gestures (one that allows wordings to be made and heard). Just as in orienting to cultural tools, a child grasps a community’s ways-with-wordings. The latter often express abstract relations which we can illustrate with modern non-literate use of reciprocal expressions. In Australian and Pacific languages, reciprocals sustain coordinating that, for speakers, is neither symbolic nor arbitrary. Further, cross-linguistic comparison shows the same ‘patchy distribution’ of reciprocals that characterizes primate tool use. Of course, we do not deny that, in many language games, people can undertake activity that makes symbolic use of wordings. In modern literate societies, abilities based on social reaching are further extended into skills that use notational practices (e.g. letters, numbers, graphics). This opens up whole new fields or domains of languaging. Yet, ostensive use of symbols is plainly a cultural invention – not a direct legacy of hominin evolution.

How to count biological minds: symbiosis, the free energy principle, and reciprocal multiscale integration

The notion of a physiological individuals has been developed and applied in the philosophy of biology to understand symbiosis, an understanding of which is key to theorising about the major transition in evolution from multi-organismality to multi-cellularity. The paper begins by asking what such symbiotic individuals can help to reveal about a possible transition in the evolution of cognition. Such a transition marks the movement from cooperating individual biological cognizers to a functionally integrated cognizing unit. Somewhere along the way, did such cognizing units simultaneously have cognizers as parts? Expanding upon the multiscale integration view of the Free Energy Principle, this paper develops an account of reciprocal integration, demonstrating how some coupled biological cognizing systems, when certain constraints are met, can result in a cognizing unit that is in ways greater than the sum of its cognizing parts. Symbiosis between V. Fischeri bacteria and the bobtail squid is used to provide an illustration this account. A novel manner of conceptualizing biological cognizers as gradient is then suggested. Lastly it is argued that the reason why the notion of ontologically nested cognizers may be unintuitive stems from the fact that our folk-psychology notion of what a cognizer is has been deeply influenced by our folk-biological manner of understanding biological individuals as units of reproduction.

Origin and elaboration of a major evolutionary transition in individuality.

Obligate endosymbiosis, in which distantly related species integrate to form a single replicating individual, represents a major evolutionary transition in individuality1-3. Although such transitions are thought to increase biological complexity1,2,4-6, the evolutionary and developmental steps that lead to integration remain poorly understood. Here we show that obligate endosymbiosis between the bacteria Blochmannia and the hyperdiverse ant tribe Camponotini7-11 originated and also elaborated through radical alterations in embryonic development, as compared to other insects. The Hox genes AbdominalA (abdA) and Ultrabithorax (Ubx)-which, in arthropods, normally function to differentiate abdominal and thoracic segments after they form-were rewired to also regulate germline genes early in development. Consequently, the mRNAs and proteins of these Hox genes are expressed maternally and colocalize at a subcellular level with those of germline genes in the germplasm and three novel locations in the freshly laid egg. Blochmannia bacteria then selectively regulate these mRNAs and proteins to make each of these four locations functionally distinct, creating a system of coordinates in the embryo in which each location performs a different function to integrate Blochmannia into the Camponotini. Finally, we show that the capacity to localize mRNAs and proteins to new locations in the embryo evolved before obligate endosymbiosis and was subsequently co-opted by Blochmannia and Camponotini. This pre-existing molecular capacity converged with a pre-existing ecological mutualism12,13 to facilitate both the horizontal transfer10 and developmental integration of Blochmannia into Camponotini. Therefore, the convergence of pre-existing molecular capacities and ecological interactions-as well as the rewiring of highly conserved gene networks-may be a general feature that facilitates the origin and elaboration of major transitions in individuality.

Towards a general theory of the major cooperative evolutionary transitions

Major Cooperative Evolutionary Transitions occur when smaller-scale entities cooperate together to give rise to larger-scale entities that evolve and adapt as coherent wholes. Key examples of cooperative transitions are the emergence of the complex eukaryote cell from communities of simpler cells, the transition from eukaryote cells to multicellular organisms, and the organization of humans into complex, modern societies. A number of attempts have been made to develop a general theory of the major cooperative transitions. This paper begins by critiquing key aspects of these previous attempts. Largely, these attempts comprise poorly-integrated collections of separate models that were each originally developed to explain particular transitions. In contrast, this paper sets out to identify processes that are common to all cooperative transitions. It develops an alternative theoretical framework known as Management Theory. This general framework suggests that all major cooperative transitions are the result of the emergence of powerful, evolvable ‘managers’ that derive benefit from using their power to organize smaller-scale entities into larger-scale cooperatives. Management Theory is a contribution to the development of a general, “all levels” understanding of major cooperative transitions that is capable of identifying those features that are level-specific, those that are common across levels and those that are involved in trends across levels.

Insights into skull evolution in fossorial snakes, as revealed by the cranial morphology of Atractaspis irregularis (Serpentes: Colubroidea).

Comparative osteological analyses of extant organisms provide key insight into major evolutionary transitions and phylogenetic hypotheses. This is especially true for snakes, given their unique morphology relative to other squamates and the persistent controversy regarding their evolutionary origins. However, the osteology of several major snake groups remains undescribed, thus hindering efforts to accurately reconstruct the phylogeny of snakes. One such group is the Atractaspididae, a family of fossorial colubroids. We herein present the first detailed description of the atractaspidid skull, based on fully segmented micro-computed tomography (micro-CT) scans of Atractaspis irregularis. The skull of Atractaspis presents a highly unique morphology influenced by both fossoriality and paedomorphosis. This paedomorphosis is especially evident in the jaws, palate, and suspensorium, the major elements associated with macrostomy (large-gaped feeding in snakes). Comparison to scolecophidians-a group of blind, fossorial, miniaturized snakes-in turn sheds light on current hypotheses of snake phylogeny. Features of both the naso-frontal joint and the morphofunctional system related to macrostomy refute the traditional notion that scolecophidians are fundamentally different from alethinophidians (all other extant snakes). Instead, these features support the controversial hypothesis of scolecophidians as "regressed alethinophidians," in contrast to their traditional placement as the earliest-diverging snake lineage. We propose that Atractaspis and scolecophidians fall along a morphological continuum, characterized by differing degrees of paedomorphosis. Altogether, a combination of heterochrony and miniaturization provides a mechanism for the derivation of the scolecophidian skull from an ancestral fossorial alethinophidian morphotype, exemplified by the nonminiaturized and less extreme paedomorph Atractaspis.