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"Nicholls, James A."
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Coevolutionary arms race versus host defense chase in a tropical herbivore–plant system
2017
Coevolutionary models suggest that herbivores drive diversification and community composition in plants. For herbivores, many questions remain regarding how plant defenses shape host choice and community structure. We addressed these questions using the tree genus Inga and its lepidopteran herbivores in the Amazon. We constructed phylogenies for both plants and insects and quantified host associations and plant defenses. We found that similarity in herbivore assemblages between Inga species was correlated with similarity in defenses. There was no correlation with phylogeny, a result consistent with our observations that the expression of defenses in Inga is independent of phylogeny. Furthermore, host defensive traits explained 40% of herbivore community similarity. Analyses at finer taxonomic scales showed that different lepidopteran clades select hosts based on different defenses, suggesting taxon-specific histories of herbivore–host plant interactions. Finally, we compared the phylogeny and defenses of Inga to phylogenies for the major lepidopteran clades. We found that closely related herbivores fed on Inga with similar defenses rather than on closely related plants. Together, these results suggest that plant defenses might be more evolutionarily labile than the herbivore traits related to host association. Hence, there is an apparent asymmetry in the evolutionary interactions between Inga and its herbivores. Although plants may evolve under selection by herbivores, we hypothesize that herbivores may not show coevolutionary adaptations, but instead “chase” hosts based on the herbivore’s own traits at the time that they encounter a new host, a pattern more consistent with resource tracking than with the arms race model of coevolution.
Journal Article
Sweet Tetra-Trophic Interactions
by
Stone, Graham N.
,
Nicholls, James A.
,
Melika, George
in
Animals
,
Correlation analysis
,
Defense mechanisms
2017
Many herbivores employ reward-based mutualisms with ants to gain protection from natural enemies. We examine the evolutionary dynamics of a tetra-trophic interaction in which gall wasp herbivores induce their host oaks to produce nectar-secreting galls, which attract ants that provide protection from parasitoids. We show that, consistent with other gall defensive traits, nectar secretion has evolved repeatedly across the oak gall wasp tribe and also within a single genus (Disholcaspis) that includes many nectar-inducing species. Once evolved, nectar secretion is never lost in Disholcaspis, consistent with high defensive value of this trait. We also show that evolution of nectar secretion is correlated with a transition from solitary to aggregated oviposition, resulting in clustered nectar-secreting galls, which produce a resource that ants can more easily monopolize. Such clustering is commonly seen in ant guard mutualisms. We suggest that correlated evolution between maternal oviposition and larval nectar induction traits has enhanced the effectiveness of this gall defense strategy.
Journal Article
Using targeted enrichment of nuclear genes to increase phylogenetic resolution in the neotropical rain forest genus Inga (Leguminosae: Mimosoideae)
by
Kidner, Catherine A.
,
Koenen, Erik J. M.
,
Stone, Graham N.
in
Algorithms
,
Bayesian analysis
,
Biological evolution
2015
Evolutionary radiations are prominent and pervasive across many plant lineages in diverse geographical and ecological settings; in neotropical rainforests there is growing evidence suggesting that a significant fraction of species richness is the result of recent radiations. Understanding the evolutionary trajectories and mechanisms underlying these radiations demands much greater phylogenetic resolution than is currently available for these groups. The neotropical tree genus Inga (Leguminosae) is a good example, with ~300 extant species and a crown age of 2-10 MY, yet over 6 kb of plastid and nuclear DNA sequence data gives only poor phylogenetic resolution among species. Here we explore the use of larger-scale nuclear gene data obtained though targeted enrichment to increase phylogenetic resolution within Inga. Transcriptome data from three Inga species were used to select 264 nuclear loci for targeted enrichment and sequencing. Following quality control to remove probable paralogs from these sequence data, the final dataset comprised 259,313 bases from 194 loci for 24 accessions representing 22 Inga species and an outgroup (Zygia). Bayesian phylogenies reconstructed using either all loci concatenated or a gene-tree/species-tree approach yielded highly resolved phylogenies. We used coalescent approaches to show that the same targeted enrichment data also have significant power to discriminate among alternative within-species population histories within the widespread species I. umbellifera. In either application, targeted enrichment simplifies the informatics challenge of identifying orthologous loci associated with de novo genome sequencing. We conclude that targeted enrichment provides the large volumes of phylogenetically-informative sequence data required to resolve relationships within recent plant species radiations, both at the species level and for within-species phylogeographic studies.
Journal Article
Extreme Host Plant Conservatism During at Least 20 Million Years of Host Plant Pursuit by Oak Gallwasps
by
Pierro, Erica di
,
Melika, George
,
Stone, Graham N.
in
Animals
,
Biological Evolution
,
Biological taxonomies
2009
Diversification of insect herbivores is often associated with coevolution between plant toxins and insect countermeasures, resulting in a specificity that restricts host plant shifts. Gall inducers, however, bypass plant toxins and the factors influencing host plant associations in these specialized herbivores remain unclear. We reconstructed the evolution of host plant associations in Western Palaearctic oak gallwasps (Cynipidae: Cynipini), a species-rich lineage of specialist herbivores on oak (Quercus). (1) Bayesian analyses of sequence data for three genes revealed extreme host plant conservatism, with inferred shifts between major oak lineages (sections Cerris and Quercus) closely matching the minimum required to explain observed diversity. It thus appears that the coevolutionary demands of gall induction constrain host plant shifts, both in cases of mutualism (e.g., fig wasps, yucca moths) and parasitism (oak gallwasps). (2) Shifts between oak sections occurred independently in sexual and asexual generations of the gallwasp lifecycle, implying that these can evolve independently. (3) Western Palaearctic gallwasps associated with sections Cerris and Quercus diverged at least 20 million years ago (mya), prior to the arrival of oaks in the Western Palaearctic from Asia 5–7 mya. This implies an Asian origin for Western Palaearctic gallwasps, with independent westwards range expansion by multiple lineages.
Journal Article
Plastid phylogenomics reveals evolutionary relationships in the mycoheterotrophic orchid genus Dipodium and provides insights into plastid gene degeneration
by
Patel, Vidushi S.
,
Goedderz, Stephanie
,
Clements, Mark A.
in
Autotrophy
,
Degeneration
,
Degradation
2024
The orchid genus
Dipodium
R.Br. (Epidendroideae) comprises leafy autotrophic and leafless mycoheterotrophic species, with the latter confined to sect.
Dipodium
. This study examined plastome degeneration in
Dipodium
in a phylogenomic and temporal context. Whole plastomes were reconstructed and annotated for 24
Dipodium
samples representing 14 species and two putatively new species, encompassing over 80% of species diversity in sect.
Dipodium
. Phylogenomic analysis based on 68 plastid loci including a broad outgroup sampling across Orchidaceae found that sect.
Leopardanthus
is the sister lineage to sect.
Dipodium. Dipodium ensifolium
, the only leafy autotrophic species in sect.
Dipodium
, was found to be a sister to all leafless, mycoheterotrophic species, supporting a single evolutionary origin of mycoheterotrophy in the genus. Divergence-time estimations found that
Dipodium
arose ca. 33.3 Ma near the lower boundary of the Oligocene and that crown diversification commenced in the late Miocene, ca. 11.3 Ma. Mycoheterotrophy in the genus was estimated to have evolved in the late Miocene, ca. 7.3 Ma, in sect.
Dipodium
. The comparative assessment of plastome structure and gene degradation in
Dipodium
revealed that plastid
ndh
genes were pseudogenised or physically lost in all
Dipodium
species, including in leafy autotrophic species of both
Dipodium
sections. Levels of plastid
ndh
gene degradation were found to vary among species as well as within species, providing evidence of relaxed selection for retention of the NADH dehydrogenase complex within the genus.
Dipodium
exhibits an early stage of plastid genome degradation, as all species were found to have retained a full set of functional photosynthesis-related genes and housekeeping genes. This study provides important insights into plastid genome degradation along the transition from autotrophy to mycoheterotrophy in a phylogenomic and temporal context.
Journal Article
Chemocoding as an identification tool where morphological- and DNA-based methods fall short
by
Graham N. Stone
,
Gordon C. Younkin
,
Kyle G. Dexter
in
biodiversity
,
case studies
,
chemocoding
2018
The need for species identification and taxonomic discovery has led to the development of innovative technologies for large-scale plant identification. DNA barcoding has been useful, but fails to distinguish among many species in species-rich plant genera, particularly in tropical regions. Here, we show that chemical fingerprinting, or ‘chemocoding’, has great potential for plant identification in challenging tropical biomes.
Using untargeted metabolomics in combination with multivariate analysis, we constructed species-level fingerprints, which we define as chemocoding. We evaluated the utility of chemocoding with species that were defined morphologically and subject to next-generation DNA sequencing in the diverse and recently radiated neotropical genus Inga (Leguminosae), both at single study sites and across broad geographic scales.
Our results show that chemocoding is a robust method for distinguishing morphologically similar species at a single site and for identifying widespread species across continental-scale ranges.
Given that species are the fundamental unit of analysis for conservation and biodiversity research, the development of accurate identification methods is essential. We suggest that chemocoding will be a valuable additional source of data for a quick identification of plants, especially for groups where other methods fall short.
Journal Article
Tracking of Host Defenses and Phylogeny During the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; Argidae)
by
Kidner, Catherine A.
,
Pennington, R. T.
,
Stone, Graham N.
in
Argidae
,
Biodiversity
,
Chlorophyll
2018
Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus
throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their
hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their
hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with
is better correlated with
chemistry than with
phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of
sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in
diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.
Journal Article
Faecal metabarcoding reveals pervasive long-distance impacts of garden bird feeding
2021
Supplementary feeding of wildlife is widespread, being undertaken by more than half of households in many countries. However, the impact that these supplemental resources have is unclear, with impacts largely considered to be restricted to urban ecosystems. We reveal the pervasiveness of supplementary foodstuffs in the diet of a wild bird using metabarcoding of blue tit (
Cyanistes caeruleus
) faeces collected in early spring from a 220 km transect in Scotland with a large urbanization gradient. Supplementary foodstuffs were present in the majority of samples, with peanut (
Arachis hypogaea
) the single commonest (either natural or supplementary) dietary item. Consumption rates exhibited a distance decay from human habitation but remained high at several hundred metres from the nearest household and continued to our study limit of 1.4 km distant. Supplementary food consumption was associated with a near quadrupling of blue tit breeding density and a 5-day advancement of breeding phenology. We show that woodland bird species using supplementary food have increasing UK population trends, while species that do not, and/or are outcompeted by blue tits, are likely to be declining. We suggest that the impacts of supplementary feeding are larger and more spatially extensive than currently appreciated and could be disrupting population and ecosystem dynamics.
Journal Article
PERCHED AT THE MITO-NUCLEAR CROSSROADS: DIVERGENT MITOCHONDRIAL LINEAGES CORRELATE WITH ENVIRONMENT IN THE FACE OF ONGOING NUCLEAR GENE FLOW IN AN AUSTRALIAN BIRD
2013
Relationships among multilocus genetic variation, geography, and environment can reveal how evolutionary processes affect genomes. We examined the evolution of an Australian bird, the eastern yellow robin Eopsaltria australis, using mitochondrial (mtDNA) and nuclear (nDNA) genetic markers, and bioclimatic variables. In southeastern Australia, two divergent mtDNA lineages occur east and west of the Great Dividing Range, perpendicular to latitudinal nDNA structure. We evaluated alternative scenarios to explain this striking discordance in landscape genetic patterning. Stochastic mtDNA lineage sorting can be rejected because the mtDNA lineages are essentially distinct geographically for > 1500 km. Vicariance is unlikely: the Great Dividing Range is neither a current barrier nor was it at the Last Glacial Maximum according to species distribution modeling; nuclear gene flow inferred from coalescent analysis affirms this. Female philopatry contradicts known female-biased dispersal. Contrasting mtDNA and nDNA demographies indicate their evolutionary histories are decoupled. Distance-based redundancy analysis, in which environmental temperatures explain mtDNA variance above that explained by geographic position and isolation-by-distance, favors a nonneutral explanation for mitochondrial phylogeographic patterning. Thus, observed mito-nuclear discordance accords with environmental selection on a female-linked trait, such as mtDNA, mtDNA–nDNA interactions or genes on W-chromosome, driving mitochondrial divergence in the presence of nuclear gene flow.
Journal Article
Community impacts of anthropogenic disturbance: natural enemies exploit multiple routes in pursuit of invading herbivore hosts
by
Nicholls, James A
,
Fuentes-Utrilla, Pablo
,
Melika, George
in
Adaptation
,
Animal Systematics/Taxonomy/Biogeography
,
Animals
2010
Background
Biological invasions provide a window on the process of community assembly. In particular, tracking natural enemy recruitment to invading hosts can reveal the relative roles of co-evolution (including local adaptation) and ecological sorting. We use molecular data to examine colonisation of northern Europe by the parasitoid
Megastigmus stigmatizans
following invasions of its herbivorous oak gallwasp hosts from the Balkans. Local host adaptation predicts that invading gallwasp populations will have been tracked primarily by sympatric Balkan populations of
M. stigmatizans
(Host Pursuit Hypothesis). Alternatively, ecological sorting allows parasitoid recruitment from geographically distinct populations with no recent experience of the invading hosts (Host Shift Hypothesis). Finally, we test for long-term persistence of parasitoids introduced via human trade of their hosts' galls (Introduction Hypothesis).
Results
Polymorphism diagnostic of different southern refugial regions was present in both mitochondrial and nuclear microsatellite markers, allowing us to identify the origins of northern European invaded range
M. stigmatizans
populations. As with their hosts, some invaded range populations showed genetic variation diagnostic of Balkan sources, supporting the Host Pursuit Hypothesis. In contrast, other invading populations had an Iberian origin, unlike their hosts in northern Europe, supporting the Host Shift Hypothesis. Finally, both British and Italian
M. stigmatizans
populations show signatures compatible with the Introduction Hypothesis from eastern Mediterranean sources.
Conclusions
These data reveal the continental scale of multi-trophic impacts of anthropogenic disturbance and highlight the fact that herbivores and their natural enemies may face very different constraints on range expansion. The ability of natural enemies to exploit ecologically-similar hosts with which they have had no historical association supports a major role for ecological sorting processes in the recent assembly of these communities. The multitude of origins of invading natural enemy populations in this study emphasises the diversity of mechanisms requiring consideration when predicting consequences of other biological invasions or biological control introductions.
Journal Article