Decreases in Brain Size and Encephalization in Anatomically Modern Humans

Growth in human brain size and encephalization is well documented throughout much of prehistory and believed to be responsible for increasing cognitive faculties. Over the past 50,000 years, however, both body size and brain mass have decreased but little is known about the scaling relationship between the two. Here, changes to the human brain are examined using matched body remains to determine encephalization levels across an evolutionary timespan. The results find decreases to encephalization levels in modern humans as compared to earlier Holocene <i>H. sapiens</i> and Late Pleistocene anatomically modern <i>Homo</i>. When controlled for lean body mass, encephalization changes are isometric, suggesting that much of the declines in encephalization are driven by recent increases in obesity. A meta-review of genome-wide association studies finds some evidence for selective pressures acting on human cognitive ability, which may be an evolutionary consequence of the more than 5% loss in brain mass over the past 50,000 years.

Assessment of the evolutionary consequence of putative driver mutations in colorectal cancer with spatial multiomic data

Cancer genomic medicine relies on targeting driver genes. However, current catalogues of cancer drivers are mostly based on indirect measurements of mutation frequencies, positions or types, rather than their effect on clonal expansions in vivo. Moreover, nongenetic drivers are largely unknown, as are the epigenetic and transcriptomic effects of genetic drivers. Here we perform spatial computational inference on multiomic data with matched whole-genome sequencing, ATAC-seq and RNA-seq. Using 436 samples, we directly quantify the contribution, or lack thereof, of putative driver genes to subclonal expansions in vivo in 30 colorectal carcinomas (4-33 samples per patient, median=15). Although subclonal neutral evolution was widespread (13/26 cases with sufficient data), there were cases with clear evidence of subclonal selection (6/26) in which we measured epigenetic and transcriptomic differences between subclones in vivo. In 7/26 cases we could not distinguish between neutral or selective evolution with the available data. We identified expanding subclones that were not driven by known genetic alterations, and propose candidate epigenetic drivers. We identified the distinguishing patterns of genomic heterogeneity produced in fast, exponentially growing tumours (7/26) versus neoplasms growing only at the periphery (19/26), as well as identifying clonally intermixed (16/28 cases with sufficient data) versus segregated malignancies (10/28). Our model-based approach measures genetic and non-genetic subclonal selection, or lack thereof, in space and time and allows in vivo comparisons of the emergent phenotypic properties of subclones within human tumours.

Genetic architecture of floral traits in bee- and hummingbird-pollinated sister species of Aquilegia (columbine)

Interactions with animal pollinators have helped shape the stunning diversity of flower morphologies across the angiosperms. A common evolutionary consequence of these interactions is that some flowers have converged on suites of traits, or pollination syndromes, that attract and reward specific pollinator groups. Determining the genetic basis of these floral pollination syndromes can help us understand the processes that contributed to the diversification of the angiosperms. Here, we characterize the genetic architecture of a bee-to-hummingbird pollination shift in Aquilegia (columbine) using QTL mapping of 17 floral traits encompassing color, nectar composition, and organ morphology. In this system, we find that the genetic architectures underlying differences in floral color are quite complex, and we identify several likely candidate genes involved in anthocyanin and carotenoid floral pigmentation. Most morphological and nectar traits also have complex genetic underpinnings; however, one of the key floral morphological phenotypes, nectar spur curvature, is shaped by a single locus of large effect.

Genome evolution of a non-parasitic secondary heterotroph, the diatom Nitzschia putrida

Secondary loss of photosynthesis is observed across almost all plastid-bearing branches of the eukaryotic tree of life. However, genome-based insights into the transition from a phototroph into a secondary heterotroph have so far only been revealed for parasitic species. Free-living organisms can yield unique insights into the evolutionary consequence of the loss of photosynthesis, as the parasitic lifestyle requires specific adaptations to host environments. Here we report on the diploid genome of the free-living diatom Nitzschia putrida (35 Mbp), a non-photosynthetic osmotroph whose photosynthetic relatives contribute ca. 40% of net oceanic primary production. Comparative analyses with photosynthetic diatoms revealed that a combination of genes loss, the horizontal acquisition of genes involved in organic carbon degradation, a unique secretome and the rapid divergence of conserved gene families involved in cell wall and extracellular metabolism appear to have facilitated the lifestyle of a non-parasitic, free-living secondary heterotroph.

Genome Evolution of the Obligate Endosymbiont Buchnera aphidicola

An evolutionary consequence of uniparentally transmitted symbiosis is degradation of symbiont genomes. We use the system of aphids and their maternally inherited obligate endosymbiont, Buchnera aphidicola, to explore the evolutionary process of genome degradation. We compared complete genome sequences for 39 Buchnera strains, including 23 newly sequenced symbiont genomes from diverse aphid hosts. We reconstructed the genome of the most recent shared Buchnera ancestor, which contained 616 protein-coding genes, and 39 RNA genes. The extent of subsequent gene loss varied across lineages, resulting in modern genomes ranging from 412 to 646 kb and containing 354–587 protein-coding genes. Loss events were highly nonrandom across loci. Genes involved in replication, transcription, translation, and amino acid biosynthesis are largely retained, whereas genes underlying ornithine biosynthesis, stress responses, and transcriptional regulation were lost repeatedly. Aside from losses, gene order is almost completely stable. The main exceptions involve movement between plasmid and chromosome locations of genes underlying tryptophan and leucine biosynthesis and supporting nutrition of aphid hosts. This set of complete genomes enabled tests for signatures of positive diversifying selection. Of 371 Buchnera genes tested, 29 genes show strong support for ongoing positive selection. These include genes encoding outer membrane porins that are expected to be involved in direct interactions with hosts. Collectively, these results indicate that extensive genome reduction occurred in the ancestral Buchnera prior to aphid diversification and that reduction has continued since, with losses greater in some lineages and for some loci.

Unravelling the macro-evolutionary ecology of fish–jellyfish associations: life in the ‘gingerbread house’

Fish–jellyfish interactions are important factors contributing to fish stock success. Jellyfish can compete with fish for food resources, or feed on fish eggs and larvae, which works to reduce survivorship and recruitment of fish species. However, jellyfish also provide habitat and space for developing larval and juvenile fish which use their hosts as means of protection from predators and feeding opportunities, helping to reduce fish mortality and increase recruitment. Yet, relatively little is known about the evolutionary dynamics and drivers of such associations which would allow for their more effective incorporation into ecosystem models. Here, we found that jellyfish association is a probable adaptive anti-predator strategy for juvenile fish, more likely to evolve in benthic (fish living on the sea floor), benthopelagic (fish living just above the bottom of the seafloor), and reef-associating species than those adapted to other marine habitats. We also found that jellyfish association likely preceded the evolution of a benthic, benthopelagic, and reef-associating lifestyle rather than its evolutionary consequence, as we originally hypothesized. Considering over two-thirds of the associating fish identified here are of economic importance, and the wide-scale occurrence and diversity of species involved, it is clear the formation of fish–jellyfish associations is an important but complex process in relation to the success of fish stocks globally.

Fighting and mating success in giant Australian cuttlefish is influenced by behavioural lateralization

Behavioural lateralization is widespread. Yet, a fundamental question remains, how can lateralization be evolutionary stable when individuals lateralized in one direction often significantly outnumber individuals lateralized in the opposite direction? A recently developed game theory model predicts that fitness consequences which occur during intraspecific interactions may be driving population-level lateralization as an evolutionary stable strategy. This model predicts that: (i) minority-type individuals exist because they are more likely to adopt unpredictable fighting behaviours during competitive interactions (e.g. fighting); and (ii) majority-type individuals exist because there is a fitness advantage in having their biases synchronized with other conspecifics during interactions that require coordination (e.g. mating). We tested these predictions by investigating biases in giant Australian cuttlefish during fighting and mating interactions. During fighting, most male cuttlefish favoured the left eye and these males showed higher contest escalation; but minority-type individuals with a right-eye bias achieved higher fighting success. During mating interactions, most male cuttlefish favoured the left eye to inspect females. Furthermore, most male cuttlefish approached the female's right side during a mating attempt and these males achieved higher mating success. Our data support the hypothesis that population-level biases are an evolutionary consequence of the fitness advantages involved in intraspecific interactions.

Does climate warming influence sexual chemical signaling?

Global climate is changing at a rapid pace and the pivotal question is if the rate and extent of species’ responses to stressful events enable them to persist in a changing world. Although the consequences of rapid environmental changes on animal life-history traits are receiving considerable attention, our understanding of how temperature fluctuations affect sexual chemical communication in animals is scarce. Male-female interactions often depend on pheromone detectability and sudden shifts in environmental temperature are expected to disrupt communication between potential mates. Whether organisms can adapt to temperature-induced changes at both signaller and receiver levels is virtually unexplored. In this perspective paper, we first provide a broad overview of the sex pheromone pathway, from biosynthesis to detection, and outline the importance of chemical-based mate choice. Finally, through several study cases, we highlight how thermal stress may interfere with chemical communication between the sexes, and discuss the potential evolutionary consequence of temperature stress.

Testing the retroelement invasion hypothesis for the emergence of the ancestral eukaryotic cell

Phylogenetic evidence suggests that the invasion and proliferation of retroelements, selfish mobile genetic elements that copy and paste themselves within a host genome, was one of the early evolutionary events in the emergence of eukaryotes. Here we test the effects of this event by determining the pressures retroelements exert on simple genomes. We transferred two retroelements, human LINE-1 and the bacterial group II intron Ll.LtrB, into bacteria, and find that both are functional and detrimental to growth. We find, surprisingly, that retroelement lethality and proliferation are enhanced by the ability to perform eukaryotic-like nonhomologous end-joining (NHEJ) DNA repair. We show that the only stable evolutionary consequence in simple cells is maintenance of retroelements in low numbers, suggesting how retrotransposition rates and costs in early eukaryotes could have been constrained to allow proliferation. Our results suggest that the interplay between NHEJ and retroelements may have played a fundamental and previously unappreciated role in facilitating the proliferation of retroelements, elements of which became the ancestors of the spliceosome components in eukaryotes.

Individual selection leads to collective efficiency through coordination

Social interactions involving coordination between individuals are subject to an “evolutionary trap.” Once a suboptimal strategy has evolved, mutants playing an alternative strategy are counterselected because they fail to coordinate with the majority. This creates a detrimental situation from which evolution cannot escape, preventing the evolution of efficient collective behaviours. Here, we study this problem using the framework of evolutionary robotics. We first confirm the existence of an evolutionary trap in a simple setting. We then, however, reveal that evolution can solve this problem in a more realistic setting where individuals need to coordinate with one another. In this setting, robots evolve an ability to adapt plastically their behaviour to one another, as this improves the efficiency of their interaction. This ability has an unintended evolutionary consequence: a genetic mutation affecting one individual’s behaviour also indirectly alters their partner’s behaviour because the two individuals influence one another. As a consequence of this indirect genetic effect, pairs of partners can virtually change strategy together with a single mutation, and the evolutionary barrier between alternative strategies disappears. This finding reveals a general principle that could play a role in nature to smoothen the transition to efficient collective behaviours in all games with multiple equilibriums.