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

Microbiota play a central role in the functioning of multicellular life, yet understanding their inheritance during host evolutionary history remains an important challenge. Symbiotic microorganisms are either acquired from the environment during the life of the host (i.e. environmental acquisition), transmitted across generations with a faithful association with their hosts (i.e. strict vertical transmission), or transmitted with occasional host switches (i.e. vertical transmission with horizontal switches). These different modes of inheritance affect microbes' diversification, which at the two extremes can be independent from that of their associated host or follow host diversification. The few existing quantitative tools for investigating the inheritance of symbiotic organisms rely on cophylogenetic approaches, which require knowledge of both host and symbiont phylogenies, and are therefore often not well adapted to DNA metabarcoding microbial data. Here, we develop a model-based framework for identifying vertically transmitted microbial taxa. We consider a model for the evolution of microbial sequences on a fixed host phylogeny that includes vertical transmission and horizontal host switches. This model allows estimating the number of host switches and testing for strict vertical transmission and independent evolution. We test our approach using simulations. Finally, we illustrate our framework on gut microbiota high-throughput sequencing data of the family Hominidae and identify several microbial taxonomic units, including fibrolytic bacteria involved in carbohydrate digestion, that tend to be vertically transmitted.

Interspecific interactions, including host-symbiont associations, can profoundly affect the evolution of the interacting species. Given the phylogenies of host and symbiont clades and knowledge of which host species interact with which symbiont, two questions are often asked: "Do closely related hosts interact with closely related symbionts?" and "Do host and symbiont phylogenies mirror one another?." These questions are intertwined and can even collapse under specific situations, such that they are often confused one with the other. However, in most situations, a positive answer to the first question, hereafter referred to as "cophylogenetic signal," does not imply a close match between the host and symbiont phylogenies. It suggests only that past evolutionary history has contributed to shaping present-day interactions, which can arise, for example, through present-day trait matching, or from a single ancient vicariance event that increases the probability that closely related species overlap geographically. A positive answer to the second, referred to as "phylogenetic congruence," is more restrictive as it suggests a close match between the two phylogenies, which may happen, for example, if symbiont diversification tracks host diversification or if the diversifications of the two clades were subject to the same succession of vicariance events. Here we apply a set of methods (ParaFit, PACo, and eMPRess), whose significance is often interpreted as evidence for phylogenetic congruence, to simulations under 3 biologically realistic scenarios of trait matching, a single ancient vicariance event, and phylogenetic tracking with frequent cospeciation events. The latter is the only scenario that generates phylogenetic congruence, whereas the first 2 generate a cophylogenetic signal in the absence of phylogenetic congruence. We find that tests of global-fit methods (ParaFit and PACo) are significant under the 3 scenarios, whereas tests of event-based methods (eMPRess) are only significant under the scenario of phylogenetic tracking. Therefore, significant results from global-fit methods should be interpreted in terms of cophylogenetic signal and not phylogenetic congruence; such significant results can arise under scenarios when hosts and symbionts had independent evolutionary histories. Conversely, significant results from event-based methods suggest a strong form of dependency between hosts and symbionts evolutionary histories. Clarifying the patterns detected by different cophylogenetic methods is key to understanding how interspecific interactions shape and are shaped by evolution.

Humans are uniquely unique, in terms of the extreme differences between them and other living organisms, and the impact they are having on the biosphere. The evolution of humans can be seen, as has been proposed, as one of the major transitions in evolution, on a par with the origins of multicellular organisms or the eukaryotic cell (Maynard Smith & Szathmáry 1997 Major transitions in evolution). Major transitions require the evolution of greater complexity and the emergence of new evolutionary levels or processes. Does human evolution meet these conditions? I explore the diversity of evidence on the nature of transitions in human evolution. Four levels of transition are proposed-baseline, novel taxa, novel adaptive zones and major transitions-and the pattern of human evolution considered in the light of these. The primary conclusions are that changes in human evolution occur continuously and cumulatively; that novel taxa and the appearance of new adaptations are not clustered very tightly in particular periods, although there are three broad transitional phases (Pliocene, Plio-Pleistocene and later Quaternary). Each phase is distinctive, with the first based on ranging and energetics, the second on technology and niche expansion, and the third on cognition and cultural processes. I discuss whether this constitutes a 'major transition' in the context of the evolutionary processes more broadly; the role of behaviour in evolution; and the opportunity provided by the rich genetic, phenotypic (fossil morphology) and behavioural (archaeological) record to examine in detail major transitions and the microevolutionary patterns underlying macroevolutionary change. It is suggested that the evolution of the hominin lineage is consistent with a mosaic pattern of change.This article is part of the themed issue 'Major transitions in human evolution'.

Bacterial endosymbionts are widespread across several insect orders and are involved in interactions ranging from obligate mutualism to reproductive parasitism. Candidatus Blochmannia gen. nov. (Blochmannia) is an obligate bacterial associate of Camponotus and related ant genera (Hymenoptera: Formicidae). The occurrence of Blochmannia in all Camponotus species sampled from field populations and its maternal transmission to host offspring suggest that this bacterium is engaged in a long-term, stable association with its ant hosts. However, evidence for cospeciation in this system is equivocal because previous phylogenetic studies were based on limited gene sampling, lacked statistical analysis of congruence, and have even suggested host switching. We compared phylogenies of host genes (the nuclear EF-1alphaF2 and mitochondrial COI/II) and Blochmannia genes (16S ribosomal DNA [rDNA], groEL, gidA, and rpsB), totaling more than 7 kilobases for each of 16 Camponotus species. Each data set was analyzed using maximum likelihood and Bayesian phylogenetic reconstruction methods. We found minimal conflict among host and symbiont phylogenies, and the few areas of discordance occurred at deep nodes that were poorly supported by individual data sets. Concatenated protein-coding genes produced a very well-resolved tree that, based on the Shimodaira-Hasegawa test, did not conflict with any host or symbiont data set. Correlated rates of synonymous substitution (d(S)) along corresponding branches of host and symbiont phylogenies further supported the hypothesis of cospeciation. These findings indicate that Blochmannia-Camponotus symbiosis has been evolutionarily stable throughout tens of millions of years. Based on inferred divergence times among the ant hosts, we estimated rates of sequence evolution of Blochmannia to be approximately 0.0024 substitutions per site per million years (s/s/MY) for the 16S rDNA gene and approximately 0.1094 s/s/MY at synonymous positions of the genes sampled. These rates are several-fold higher than those for related bacteria Buchnera aphidicola and Escherichia coli. Phylogenetic congruence among Blochmannia genes indicates genome stability that typifies primary endosymbionts of insects.

In parasites with mixed modes of transmission, ecological conditions may determine the relative importance of vertical and horizontal transmission for parasite fitness. This may lead to differential selection pressure on the efficiency of the two modes of transmission and on parasite virulence. In populations with high birth rates, increased opportunities for vertical transmission may select for higher vertical transmissibility and possibly lower virulence. We tested this idea in experimental populations of the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. Serial dilution produced constant host population growth and frequent vertical transmission. Consistent with predictions, evolved parasites from this "high-growth" treatment had higher fidelity of vertical transmission and lower virulence than parasites from host populations constantly kept near their carrying capacity ("low-growth treatment"). High-growth parasites also produced fewer, but more infectious horizontal transmission stages, suggesting the compensation of trade-offs between vertical and horizontal transmission components in this treatment. These results illustrate how environmentally driven changes in host demography can promote evolutionary divergence of parasite life history and transmission strategies.

The role of species’ interactions in structuring biological communities remains unclear. Mutualistic symbioses, involving close positive interactions between two distinct organismal lineages, provide an excellent means to explore the roles of both evolutionary and ecological processes in determining how positive interactions affect community structure. In this study, we investigate patterns of co-diversification between fungi and algae for a range of New Zealand lichens at the community, genus, and species levels and explore explanations for possible patterns related to spatial scale and pattern, taxonomic diversity of the lichens considered, and the level sampling replication. We assembled six independent datasets to compare patterns in phylogenetic congruence with varied spatial extent of sampling, taxonomic diversity and level of specimen replication. For each dataset, we used the DNA sequences from the ITS regions of both the fungal and algal genomes from lichen specimens to produce genetic distance matrices. Phylogenetic congruence between fungi and algae was quantified using distance-based redundancy analysis and we used geographic distance matrices in Moran’s eigenvector mapping and variance partitioning to evaluate the effects of spatial variation on the quantification of phylogenetic congruence. Phylogenetic congruence was highly significant for all datasets and a large proportion of variance in both algal and fungal genetic distances was explained by partner genetic variation. Spatial variables, primarily at large and intermediate scales, were also important for explaining genetic diversity patterns in all datasets. Interestingly, spatial structuring was stronger for fungal than algal genetic variation. As the spatial extent of the samples increased, so too did the proportion of explained variation that was shared between the spatial variables and the partners’ genetic variation. Different lichen taxa showed some variation in their phylogenetic congruence and spatial genetic patterns and where greater sample replication was used, the amount of variation explained by partner genetic variation increased. Our results suggest that the phylogenetic congruence pattern, at least at small spatial scales, is likely due to reciprocal co-adaptation or co-dispersal. However, the detection of these patterns varies among different lichen taxa, across spatial scales and with different levels of sample replication. This work provides insight into the complexities faced in determining how evolutionary and ecological processes may interact to generate diversity in symbiotic association patterns at the population and community levels. Further, it highlights the critical importance of considering sample replication, taxonomic diversity and spatial scale in designing studies of co-diversification.

For the last three decades, evolutionary biologists have sought to understand which factors modulate the evolution of parasite virulence. Although theory has identified several of these modulators, their effect has seldom been analysed experimentally. We investigated the role of two such major factors—the mode of transmission, and host adaptation in response to parasite evolution—in the evolution of virulence of the plant virus Cucumber mosaic virus (CMV) in its natural host Arabidopsis thaliana. To do so, we serially passaged three CMV strains under strict vertical and strict horizontal transmission, alternating both modes of transmission. We quantified seed (vertical) transmission rate, virus accumulation, effect on plant growth and virulence of evolved and non-evolved viruses in the original plants and in plants derived after five passages of vertical transmission. Our results indicated that vertical passaging led to adaptation of the virus to greater vertical transmission, which was associated with reductions of virus accumulation and virulence. On the other hand, horizontal serial passages did not significantly modify virus accumulation and virulence. The observed increases in CMV seed transmission, and reductions in virus accumulation and virulence in vertically passaged viruses were due also to reciprocal host adaptation during vertical passages, which additionally reduced virulence and multiplication of vertically passaged viruses. This result is consistent with plant-virus co-evolution. Host adaptation to vertically passaged viruses was traded-off against reduced resistance to the non-evolved viruses. Thus, we provide evidence of the key role that the interplay between mode of transmission and host-parasite co-evolution has in determining the evolution of virulence.

A major transition in evolution (MTE) is complete when both partners become so dependent on each other that they reproduce as a unit. Typically, the smaller partner becomes a passenger transmitted from one generation of its host to the next along with the genes of the host, as happens in mitochondria and chloroplasts. What happens in lichens is complicated. At least 27 modes of reproduction are known, of which 13 involve a dispersal unit that contains the cells of an alga encased in fungus. In the remaining 14, the unit is a lone fungus that must find free-living algal cells to make a new lichen. As far as major transitions go, the 27 modes of lichen reproduction can be divided into just two kinds, depending on whether the alga is transmitted vertically (by inheritance) or horizontally (acquired from the environment). Only the lichens with vertical transmission have completed the transformation to a new individual. MTEs have occurred in many other symbioses, such as in insects that carry nutrient-supplying bacteria in a specialized organ called the bacteriome. There is a continuum of benefit in symbiosis, from cooperation (mutualism) at one end to theft (parasitism) at the other. It’s hard to tell where the bacteriome of insects sits on this continuum because the bacteria are so completely controlled by the insect host. But experiments suggest that, if allowed to, bacteria would multiply much faster than they can in the bacteriome and that therefore they are the prisoners not mutualists of insects.

Ecological conditions may greatly affect the relative importance of vertical and horizontal transmission, in particular for parasites with a mixed mode of transmission. Resource availability is one important environmental factor, affecting host growth and fecundity, but also the parasite’s own development. The consequences for the potential of vertical and horizontal transmission and for the evolution of transmission mode are largely unknown. We let the mixed-mode microsporidian parasite Edhazardia aedis evolve on its mosquito host Aedes aegypti under high-food or low-food conditions, representing permissive and restricted conditions. These alter the timing of development of infected larvae and thereby the probabilities for the parasites to enter the vertical or horizontal transmission pathways. After 10 generations, evolved parasites were assayed under the two food levels. There was an ecological trade-off between transmission modes, mediated by nutrient effects on host development, resulting in a higher vertical transmission (VT) potential under high-food and a higher horizontal transmission (HT) potential under low-food test conditions. Evolution under high food increased the VT potential of the parasite, particularly if it was tested at low food. This involved higher probability of carrying binucleate spores for the emerging females, greater fecundity and a longer life compared to parasites that were tested in the same conditions but had evolved under low food. The changes are related to the developmental regulation and switch in the production of two spore types, affecting investment in VT or HT. In contrast, the HT potential remained relatively unaffected by the parasite’s evolutionary history, suggesting that, within our experiential design, the VT mode evolved independently of the HT mode. Our work illustrates the possible links between resource availability, within-host developmental processes and the evolution of parasite transmission investment. Future work, theoretical and experimental, should scale up from within-host to between-host levels, including eco-evolutionary and epidemiological dynamics.

Perinatal COVID-19.

Many pathogens that are predominantly sexually transmitted can also be transmitted vertically. On the other hand, nonbeneficial pathogens that are predominantly vertically transmitted appear to be rare to absent. Many infections also exist that are only transmitted sexually. Using an empirically suggested trade-off between the horizontal and vertical transmission modes, we develop and analyze a model to study evolutionary dynamics of sterilizing, sexually transmitted infections which can also be transmitted vertically. We assume several flexible forms of the trade-off and ask under which conditions evolution in nonbeneficial pathogens favors vertical transmission, sexual transmission, or a mixture of the two. The evolutionary analysis of our model reveals a rich spectrum of evolutionary outcomes. In particular, evolution of pure sexual, pure vertical, and mixed transmission is possible, in addition to a frequent occurrence of evolutionary suicide. These outcomes can also arise via evolutionary branching and be combined in several evolutionary bistability regimes. We show that the shape of the trade-off between the two transmission modes significantly affects pathogen evolution. In particular, while vertical transmission dominates for concave and sigmoid trade-offs, sexual transmission is most commonly observed under convex trade-offs. Our analysis can shed more light on when an infection adopts a particular evolutionary behavior, and which region of the parameter space is realistic, so something about the evolutionary process itself.

The microsporidian parasite Edhazardia aedis is capable of vertical or horizontal transmission among individuals of its host, the mosquito Aedes aegypti, and either mode of transmission may follow the other. We show that following the horizontal infection of host larvae, the parasite's subsequent mode of transmission largely depends on host life history traits and their responses to different environmental conditions. In two experiments the intensity of larval exposure to infection and the amount of food available to them were simultaneously manipulated. One experiment followed the dynamics of host development and the parasite's production of spores while the other estimated the outcome of their relationship. Host life history traits varied widely across treatment conditions while those of the parasite did not. Of particular importance was the host's larval growth rate. Horizontal rather than vertical transmission by the parasite was more likely as low food and high dose conditions favoured slower larval growth rates. This pattern of transmission behaviour with host growth rate can be considered in terms of reproductive value: the potential vertical transmission success that female mosquitoes offer the parasite decreases as larval growth rates slow and makes them more attractive to exploitation for horizontal transmission (requiring host mortality). However, the lack of variation in the parasite's life history traits gave rise in some conditions to low estimates for both its vertical and horizontal transmission success. We suggest that the unresponsive behaviour of the parasite's life history traits reflects a bet-hedging strategy to reduce variance in its overall transmission success in the unpredictable environmental conditions and host larval growth rates that this parasite encounters in nature.

To consider holobionts with their hologenomes as levels of selection in evolution, there must be a continuity of partnerships between holobiont throughout generations. Microbiotas are transmitted from parent to offspring by a variety of methods, including cytoplasmic inheritance, via eggs and seeds, coprophagy (consumption of feces), close contact during and after birth, via insect vectors, and via the environment. Vertical transmission is defined as the movement of microbiota from parent to offspring without mixing with microbes in the environment. In humans, colonization of the newborn gut occurs initially via inoculation with maternal vaginal and fecal microbes when the baby transits the birth channel (vertical transmission). Breastfeeding provides an additional route of maternal vertical microbial transmission. Individuals can acquire and transfer symbionts throughout their lives, and not just during their reproductive phase. Using animal systems, including humans, it has been shown that a large fraction of bacterial species and specific strains in the microbiome are transmitted to offspring over short and long periods. It has been suggested that transmission of mutualistic symbionts and group living (animal sociality) coevolved. The large varieties in modes of transmission have an interesting implication: The fidelity of transmission of the microbiome lends a strong basis for each holobiont to be a unique biological entity, largely maintaining the uniqueness of the entity and conserving the species, from one generation to the next.

Forty-two prepubertal children presenting with anogenital (AG) warts (15 boys and 27 girls) were prospectively followed up (mean 15.9 months, SD 12.24). Most (73.8%) of these children had perianal condylomatous-type warts and 11 (26.2%) had concurrent non-genital (NG) warts. None had any other AG infections or sexually transmitted disease (STD). Twelve (28.6%) children acquired their AG warts by vertical transmission from an infected maternal birth canal, 3 (7.1%) by autoinoculation from common hand warts and 2 children (4.8%) through sexual abuse. In the remaining 25 children (59.5%) mode of acquisition of AG warts was uncertain but not thought to be sexual. Human papilloma virus (HPV) DNA (types 6/11, 16/18 or 31,33,35-31+) was detected in 10/32 (31.3%) of AG warts biopsied from these children, types 6/11 in the majority of positive biopsies (9/10). Detection of HPV DNA (types 6/11, 16/18 or 31+) in a child's AG warts was significantly associated with either vertical or sexual transmission (P < 0.02). Thirty-one children had their warts treated with a combination of scissor excision and electrocautery under general anaesthesia. Warts recurred in 10 (31.4%) of these children all within 4 months following treatment. Spontaneous resolution of AG warts was seen in 9 (21.4%) children. Of 42 children with AG warts 10 (23.8%) had at least one adult family member with AG warts, 13 (36.9%) on adult family member with another AG infection or STD, and 23 (62.2%) had a mother with cervical intraepithelial neoplasia (CIN). Twenty (47.6%) of these children had a family member with NG warts.(ABSTRACT TRUNCATED AT 250 WORDS)

Familial clustering of HTLV-1 and related diseases has been reported in Brazil. However, intrafamilial transmission of HTLV-1 based on molecular analysis has been studied only in a few communities of Japanese immigrants and African-Brazilians. To investigate the familial clustering of HTLV-1 infection and to determine the likely routes of transmission through epidemiological and genetic analyzes. Medical records of 1,759 HTLV-1+ patients from de the Center for HTLV in Salvador, Brazil, were evaluated to identify first-degree relatives previously tested for HTLV-1. Familial clustering was assumed if more than one member of the same family was HTLV-1+. LTR regions of HTLV-1 sequences were analyzed for the presence of intrafamilial polymorphisms. Family pedigrees were constructed and analyzed to infer the likely transmission routes of HTLV-1. In 154 patients at least one other family member had tested positive for HTLV-1 (a total of 182 first-degree relatives). Of the 91 couples (182 individuals), 51.6% were breastfed, and 67.4% reported never using a condom. Of the 42 mother-child pairs, 23.8% had a child aged 13 years or younger; all mothers reported breastfeeding their babies. Pedigrees of families with 4 or more members suggests that vertical transmission is a likely mode of transmission in three families. Three families may have had both vertical and sexual transmission routes for HTLV-1. The genetic signatures of the LTR region of 8 families revealed 3 families with evidence of vertical transmission, another 3 families (spouses) with sexual transmission, and one family with both transmission routes. HTLV-1 sequences belonged to Cosmopolitan subtype HTLV-1a Transcontinental subgroup A. Sexual and vertical transmission routes contribute to the intrafamilial spread of HTLV-1 in the state of Bahia.