Douglas W. Yu

Environmental DNA for wildlife biology and biodiversity monitoring

Extraction and identification of DNA from an environmental sample has proven noteworthy recently in detecting and monitoring not only common species, but also those that are endangered, invasive, or elusive. Particular attributes of so-called environmental DNA (eDNA) analysis render it a potent tool for elucidating mechanistic insights in ecological and evolutionary processes. Foremost among these is an improved ability to explore ecosystem-level processes, the generation of quantitative indices for analyses of species, community diversity, and dynamics, and novel opportunities through the use of time-serial samples and unprecedented sensitivity for detecting rare or difficult-to-sample taxa. Although technical challenges remain, here we examine the current frontiers of eDNA, outline key aspects requiring improvement, and suggest future developments and innovations for research.

Is beauty in the eye of the beholder

Why are some humans considered more beautiful than others? Theory suggests that sexually reproducing organisms should choose mates displaying characters indicative of high genotypic or phenotypic quality. Attraction to beautiful individuals may therefore be an adaptation for choosing high-quality mates. Culturally invariant standards of beauty in humans have been taken as evidence favouring such an adaptationist explanation of attraction; however, if standards of beauty are instead no more than artefacts of culture, they should vary across cultures. Here we show that male preference for women with a low waist-to-hip ratio (WHR) is not culturally universal, as had previously been assumed.

Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding

To manage and conserve biodiversity, one must know what is being lost, where, and why, as well as which remedies are likely to be most effective. Metabarcoding technology can characterise the species compositions of mass samples of eukaryotes or of environmental DNA. Here, we validate metabarcoding by testing it against three high-quality standard data sets that were collected in Malaysia (tropical), China (subtropical) and the United Kingdom (temperate) and that comprised 55,813 arthropod and bird specimens identified to species level with the expenditure of 2,505 person-hours of taxonomic expertise. The metabarcode and standard data sets exhibit statistically correlated alpha- and beta-diversities, and the two data sets produce similar policy conclusions for two conservation applications: restoration ecology and systematic conservation planning. Compared with standard biodiversity data sets, metabarcoded samples are taxonomically more comprehensive, many times quicker to produce, less reliant on taxonomic expertise and auditable by third parties, which is essential for dispute resolution.

The Competition‐Colonization Trade‐off Is Dead; Long Live the Competition‐Colonization Trade‐off

When applied at the individual patch level, the classic competition‐colonization models of species coexistence assume that propagules of superior competitors can displace adults of inferior competitors (displacement competition). But if adults are invulnerable to displacement by propagules (as trees are to seeds), and propagules compete to replace adults that die for reasons independent of the outcome of juvenile competition (a lottery system), a competition‐colonization trade‐off alone is not able to produce coexistence. However, we show that coexistence is possible if patch density varies spatially, such that it becomes a niche axis. We also show how a dispersal‐fecundity trade‐off can partition variation in patch density. We discuss the application of these models to empirical systems. An important implication of communities coexisting via variation in patch density is that the amount of habitat loss necessarily interacts with the pattern of loss in affecting extinctions, invasions, and coexistence, in contrast to displacement competition models, for which the spatial pattern of loss is not important or is less important. Finally, with respect to mechanisms promoting coexistence, we suggest that trade‐offs between different stages of colonization could be far more common in nature than a trade‐off between competitive ability and colonization ability.

A castration parasite of an ant–plant mutualism

Exploring the factors governing the maintenance and breakdown of cooperation between mutualists is an intriguing and enduring problem for evolutionary ecology, and symbioses between ants and plants can provide useful experimental models for such studies. Hundreds of tropical plant species have evolved structures to house and feed ants, and these ant–plant symbioses have long been considered classic examples of mutualism. Here, we report that the primary ant symbiont, Allomerus cf. demerarae, of the most abundant ant–plant found in south–east Peru, Cordia nodosa Lam., castrates its host plant. Allomerus workers protect new leaves and their associated domatia from herbivory, but destroy flowers, reducing fruit production to zero in most host plants. Castrated plants occupied by Allomerus provide more domatia for their associated ants than plants occupied by three species of Azteca ants that do not castrate their hosts. Allomerus colonies in larger plants have higher fecundity. As a consequence, Allomerus appears to benefit from its castration behaviour, to the detriment of C. nodosa. The C. nodosa–ant system exhibits none of the retaliatory or filtering mechanisms shown to stabilize cheating in other cooperative systems, and appears to persist because some of the plants, albeit a small minority, are inhabited by the three species of truly mutualistic Azteca ants.

A mixed community of actinomycetes produce multiple antibiotics for the fungus farming ant Acromyrmex octospinosus

BackgroundAttine ants live in an intensely studied tripartite mutualism with the fungus Leucoagaricus gongylophorus, which provides food to the ants, and with antibiotic-producing actinomycete bacteria. One hypothesis suggests that bacteria from the genus Pseudonocardia are the sole, co-evolved mutualists of attine ants and are transmitted vertically by the queens. A recent study identified a Pseudonocardia-produced antifungal, named dentigerumycin, associated with the lower attine Apterostigma dentigerum consistent with the idea that co-evolved Pseudonocardia make novel antibiotics. An alternative possibility is that attine ants sample actinomycete bacteria from the soil, selecting and maintaining those species that make useful antibiotics. Consistent with this idea, a Streptomyces species associated with the higher attine Acromyrmex octospinosus was recently shown to produce the well-known antifungal candicidin. Candicidin production is widespread in environmental isolates of Streptomyces, so this could either be an environmental contaminant or evidence of recruitment of useful actinomycetes from the environment. It should be noted that the two possibilities for actinomycete acquisition are not necessarily mutually exclusive.ResultsIn order to test these possibilities we isolated bacteria from a geographically distinct population of A. octospinosus and identified a candicidin-producing Streptomyces species, which suggests that they are common mutualists of attine ants, most probably recruited from the environment. We also identified a Pseudonocardia species in the same ant colony that produces an unusual polyene antifungal, providing evidence for co-evolution of Pseudonocardia with A. octospinosus.ConclusionsOur results show that a combination of co-evolution and environmental sampling results in the diversity of actinomycete symbionts and antibiotics associated with attine ants.

Exploiting sparseness in de novo genome assembly

BackgroundThe very large memory requirements for the construction of assembly graphs for de novo genome assembly limit current algorithms to super-computing environments.MethodsIn this paper, we demonstrate that constructing a sparse assembly graph which stores only a small fraction of the observed k- mers as nodes and the links between these nodes allows the de novo assembly of even moderately-sized genomes (~500 M) on a typical laptop computer.ResultsWe implement this sparse graph concept in a proof-of-principle software package, SparseAssembler, utilizing a new sparse k- mer graph structure evolved from the de Bruijn graph. We test our SparseAssembler with both simulated and real data, achieving ~90% memory savings and retaining high assembly accuracy, without sacrificing speed in comparison to existing de novo assemblers.

AN EMPIRICAL MODEL OF SPECIES COEXISTENCE IN A SPATIALLY STRUCTURED ENVIRONMENT

Ecological theory has long supported the idea that species coexistence in a homogeneous habitat is promoted by spatial structure, but empirical evidence for this hypothesis has lagged behind theory. Here we describe a Neotropical ant-plant symbiosis that is ideally suited for testing spatial models of coexistence. Two genera of ants, Allomerus cf. demerarae and three species of Azteca are specialized to live on a single species of ant-plant, Cordia nodosa, in a Western Amazonian tropical rain forest. Empirically, using census data from widely separated localities, we show that the relative colonization abilities of the two ant genera are a function of plant density. A parameterized model shows that this pattern alone is sufficiently robust to explain coexistence in the system. Census and experimental data suggest that Azteca queens are better long-distance flyers, but that Allomerus colonies are more fecund. Thus, Azteca can dominate in areas where host-plant densities are low (and parent colony-sapling distances are long), and Allomerus can dominate in areas where host-plant densities are high. Existing spatial heterogeneity in host-plant densities therefore can allow regional coexistence, and intersite dispersal can produce local mixing. In conclusion, a dispersal-fecundity trade-off appears to allow the two genera to treat spatial heterogeneity in patch density as a niche axis. This study further suggests that a spatially structured approach is essential in understanding the persistence of some mutualisms in the presence of parasites.

Economic game theory for mutualism and cooperation.

We review recent work at the interface of economic game theory and evolutionary biology that provides new insights into the evolution of partner choice, host sanctions, partner fidelity feedback and public goods. (1) The theory of games with asymmetrical information shows that the right incentives allow hosts to screen-out parasites and screen-in mutualists, explaining successful partner choice in the absence of signalling. Applications range from ant-plants to microbiomes. (2) Contract theory distinguishes two longstanding but weakly differentiated explanations of host response to defectors: host sanctions and partner fidelity feedback. Host traits that selectively punish misbehaving symbionts are parsimoniously interpreted as pre-adaptations. Yucca-moth and legume-rhizobia mutualisms are argued to be examples of partner fidelity feedback. (3) The theory of public goods shows that cooperation in multi-player interactions can evolve in the absence of assortment, in one-shot social dilemmas among non-kin. Applications include alarm calls in vertebrates and exoenzymes in microbes.

A Single Streptomyces Symbiont Makes Multiple Antifungals to Support the Fungus Farming Ant Acromyrmex octospinosus

Attine ants are dependent on a cultivated fungus for food and use antibiotics produced by symbiotic Actinobacteria as weedkillers in their fungus gardens. Actinobacterial species belonging to the genera Pseudonocardia, Streptomyces and Amycolatopsis have been isolated from attine ant nests and shown to confer protection against a range of microfungal weeds. In previous work on the higher attine Acromyrmex octospinosus we isolated a Streptomyces strain that produces candicidin, consistent with another report that attine ants use Streptomyces-produced candicidin in their fungiculture. Here we report the genome analysis of this Streptomyces strain and identify multiple antibiotic biosynthetic pathways. We demonstrate, using gene disruptions and mass spectrometry, that this single strain has the capacity to make candicidin and multiple antimycin compounds. Although antimycins have been known for >60 years we report the sequence of the biosynthetic gene cluster for the first time. Crucially, disrupting the candicidin and antimycin gene clusters in the same strain had no effect on bioactivity against a co-evolved nest pathogen called Escovopsis that has been identified in ∼30% of attine ant nests. Since the Streptomyces strain has strong bioactivity against Escovopsis we conclude that it must make additional antifungal(s) to inhibit Escovopsis. However, candicidin and antimycins likely offer protection against other microfungal weeds that infect the attine fungal gardens. Thus, we propose that the selection of this biosynthetically prolific strain from the natural environment provides A. octospinosus with broad spectrum activity against Escovopsis and other microfungal weeds.