David Nash | University of Copenhagen (original) (raw)

Papers by David Nash

Naturwissenschaften, Sep 27, 2016

Signalling is necessary for the maintenance of inter-specific mutualisms but is vulnerable to exp... more Signalling is necessary for the maintenance of inter-specific mutualisms but is vulnerable to exploitation by eavesdropping. While eavesdropping of intra-specific signals has been studied extensively, such exploitation of inter-specific signals has not been widely documented. The juvenile stages of the Australian lycaenid butterfly, Jalmenus evagoras, form an obligate association with several species of attendant ants, including Iridomyrmex mayri. Ants protect the caterpillars and pupae, and in return are rewarded with nutritious secretions. Female and male adult butterflies use ants as signals for oviposition and mate searching respectively. Our experiments reveal that two natural enemies of J. evagoras, araneid spiders and braconid parasitoid wasps, exploit ant signals as cues for increasing their foraging and oviposition success respectively. Intriguingly, selection through eavesdropping is unlikely to modify the ant signal.

Phylogenetic tree of the study species used for statistical correction of phylogenetic signal in ... more Phylogenetic tree of the study species used for statistical correction of phylogenetic signal in all analyses and for analysis of substitution rate. This tree was created from species' consensus barcode sequences using the programs "RAxML" through the "raxmlGUI v1.5b1" interface and "FigTree" (http://tree.bio.ed.ac.uk/software/figtree/). Node support is given as % bootstrap replications.

Biological Conservation, Jul 1, 2014

Assessing reintroduction schemes by comparing genetic diversity of reintroduced and source popula... more Assessing reintroduction schemes by comparing genetic diversity of reintroduced and source populations: A case study of the globally threatened large blue butterfly (Maculinea anion).

Proceedings of The Royal Society B: Biological Sciences, Sep 12, 2018

The role of specialization in diversification can be explored along two geological axes in the bu... more The role of specialization in diversification can be explored along two geological axes in the butterfly family Lycaenidae. In addition to variation in hostplant specialization normally exhibited by butterflies, the caterpillars of most Lycaenidae have symbioses with ants ranging from no interactions through to obligate and specific associations, increasing niche dimensionality in ant-associated taxa. Based on mitochondrial sequences from 8282 specimens from 967 species and 249 genera, we show that the degree of ecological specialization of lycaenid species is positively correlated with genetic divergence, haplotype diversity and an increase in isolation by distance. Nucleotide substitution rate is higher in carnivorous than phytophagous lycaenids. The effects documented here for both micro-and macroevolutionary processes could result from increased spatial segregation as a consequence of reduced connectivity in specialists, niche-based divergence or a combination of both. They could also provide an explanation for the extraordinary diversity of the Lycaenidae and, more generally, for diversity in groups of organisms with similar multi-dimensional ecological specialization.

The role of specialization in diversification is an active area of evolutionary research. One sys... more The role of specialization in diversification is an active area of evolutionary research. One system where the importance of specialization has been emphasized is in the diverse butterfly family Lycaenidae. In addition to variation in host-plant specialization normally exhibited by butterflies, the caterpillars of most Lycaenidae have symbioses with ants ranging from no interactions through to obligate and specific associations, increasing niche dimensionality in ant-associated taxa. Based on mitochondrial sequences from 8282 specimens from 967 species and 249 genera, we show that the degree of ecological specialization of lycaenid species is positively correlated with genetic divergence, haplotype diversity and an increase in isolation by distance. Nucleotide substitution rate was higher in carnivorous than phytophagous lycaenids. The effects documented for both micro- and macroevolutionary processes could result from increased spatial segregation as a consequence of reduced connectivity in specialists, niche-based divergence or a combination of both. They could also provide an explanation for the extraordinary diversity of the Lycaenidae and, more generally, for diversity in groups of organisms with similar multi-dimensional ecological specialization.

Insects, Aug 20, 2020

The endangered Alcon blue butterfly (Phengaris alcon) starts its larval stage by feeding on the s... more The endangered Alcon blue butterfly (Phengaris alcon) starts its larval stage by feeding on the seeds of gentian plants, after which it completes development in the nests of suitable Myrmica ant species. Any particular population often uses more than one host ant species, and some host switching is likely. To test switching in the lab we introduced relatively strong colonies of alien Myrmica species to the arenas of weaker colonies, and to orphaned caterpillars. Most of the caterpillars were successfully readopted by alien ants, and survived well. Our results suggest higher ecological plasticity in host ant usage of this butterfly than generally thought. The Alcon blue is an iconic species, e.g., its special life cycle has featured in several high profile television and streaming media wildlife series, and the more we know about its unusual life the more we can do for its protected sites.

BMC Evolutionary Biology, Feb 25, 2015

Background: The obligate mutualism between fungus-growing ants and microbial symbionts offers exc... more Background: The obligate mutualism between fungus-growing ants and microbial symbionts offers excellent opportunities to study the specificity and stability of multi-species interactions. In addition to cultivating fungus gardens, these ants have domesticated actinomycete bacteria to defend gardens against the fungal parasite Escovopsis and possibly other pathogens. Panamanian Acromyrmex echinatior leaf-cutting ants primarily associate with actinomycetes of the genus Pseudonocardia. Colonies are inoculated with one of two vertically transmitted phylotypes (Ps1 or Ps2), and maintain the same phylotype over their lifetime. We performed a cross-fostering experiment to test whether co-adaptations between ants and bacterial phylotypes have evolved, and how this affects bacterial growth and ant prophylactic behavior after infection with Escovopsis. Results: We show that Pseudonocardia readily colonized ants irrespective of their colony of origin, but that the Ps2 phylotype, which was previously shown to be better able to maintain its monocultural integrity after workers became foragers than Ps1, reached a higher final cover when grown on its native host than on alternative hosts. The frequencies of major grooming and weeding behaviors co-varied with symbiont/host combinations, showing that ant behavior also was affected when cuticular actinomycete phylotypes were swapped. Conclusion: These results show that the interactions between leaf-cutting ants and Pseudonocardia bear signatures of mutual co-adaptation within a single ant population.

Proceedings of The Royal Society B: Biological Sciences, Mar 18, 2009

To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria (P... more To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria (Pseudonocardia) that are cultured on the ants' exoskeletons and chemical cocktails from exocrine glands, especially the metapleural glands (MG). Previous work has hypothesized that (i) Pseudonocardia antibiotics are narrow-spectrum and control a fungus (Escovopsis) that parasitizes the ants' fungal symbiont, and (ii) MG secretions have broad-spectrum activity and protect ants and brood. We assessed the relative importance of these lines of defence, and their activity spectra, by scoring abundance of visible Pseudonocardia for nine species from five genera and measuring rates of MG grooming after challenging ants with disease agents of differing virulence. Atta and Sericomyrmex have lost or greatly reduced the abundance of visible bacteria. When challenged with diverse disease agents, including Escovopsis, they significantly increased MG grooming rates and expanded the range of targets. By contrast, species of Acromyrmex and Trachymyrmex maintain abundant Pseudonocardia. When challenged, these species had lower MG grooming rates, targeted primarily to brood. More elaborate MG defences and reduced reliance on mutualistic Pseudonocardia are correlated with larger colony size among attine genera, raising questions about the efficacy of managing disease in large societies with chemical cocktails versus bacterial antimicrobial metabolites.

Proceedings of The Royal Society B: Biological Sciences, Aug 22, 2012

Ants have paired metapleural glands (MGs) to produce secretions for prophylactic hygiene. These e... more Ants have paired metapleural glands (MGs) to produce secretions for prophylactic hygiene. These exocrine glands are particularly well developed in leaf-cutting ants, but whether the ants can actively regulate MG secretion is unknown. In a set of controlled experiments using conidia of five fungi, we show that the ants adjust the amount of MG secretion to the virulence of the fungus with which they are infected. We further applied fixed volumes of MG secretion of ants challenged with constant conidia doses to agar mats of the same fungal species. This showed that inhibition halos were significantly larger for ants challenged with virulent and mild pathogens/weeds than for controls and Escovopsischallenged ants. We conclude that the MG defence system of leaf-cutting ants has characteristics reminiscent of an additional cuticular immune system, with specific and non-specific components, of which some are constitutive and others induced.

Insect Conservation and Diversity, Jun 18, 2019

Myrmica scabrinodis is one of the commonest European ant species, but field observations of varia... more Myrmica scabrinodis is one of the commonest European ant species, but field observations of variable ecology and behaviour have suggested the existence of several ecotypes or even cryptic species within this ant. To address this hypothesis, we reconstructed the molecular phylogeny of M. scabrinodis and 15 related species based on 1089 base pairs of mitochondrial genes cytochrome B (Cyt‐B) and cytochrome oxidase subunit I (COI). We show that two major lineages occur throughout Europe. The observed sequence divergence between the two M. scabrinodis lineages is similar to or greater than that observed between the other investigated species. On a local scale, the lineages are both observed at the wet and dry extremes of the overall M. scabrinodis niche distribution, but analysis of the Myrmica communities in two sympatric populations shows that lineage B tends to avoid the drier habitat patches. Our inferred phylogenetic relationship of intra‐ and inter‐specific mitochondrial lineages within the M. scabrinodis species group in general shows several inconsistencies with the presently accepted taxonomy, suggesting the potential existence of more unrecognised cryptic species. The separate status of other species is not supported, particularly the differentiation between Myrmica sabuleti and Myrmica lonae, and specimens identified as Myrmica tulinae have highly inconsistent mitochondrial haplotypes, suggesting that the morphology associated with this taxon does not reflect phylogeny. The existence of multiple lineages within M. scabrinodis, and the apparent synonymy between M. lonae and M. sabuleti has implications for the conservation of Maculinea butterflies, for which these are major hosts.

Current Biology, Sep 1, 2014

Ecological Entomology, Jul 1, 2002

1. Maculinea alcon uses three different species of Myrmica host ants along a north±south gradient... more 1. Maculinea alcon uses three different species of Myrmica host ants along a north±south gradient in Europe. Based on this geographical variation in host ant use, Elmes et al. (1994) suggested that M. alcon might consist of three or more cryptic species or host races, each using a single and different host-ant species. 2. Population-specific differences in allozyme genotypes of M. alcon in Denmark (Gadeberg & Boomsma, 1997) have suggested that genetically differentiated forms may occur in a gradient across Denmark, possibly in relation to the use of different host ants. 3. It was found that two host-ant species are indeed used as hosts in Denmark, but not in a clear-cut north±south gradient. Furthermore, specificity was not complete for many M. alcon populations. Of five populations investigated in detail, one used primarily M. rubra as a host, another exclusively used M. ruginodis, while the other three populations used both ant species. No population in Denmark used M. scabrinodis as a host, although this species was present in the habitat and is known to be a host in central and southern Europe. 4. In terms of number of parasites per nest and number of nests parasitised, M. rubra seems to be a more suitable host in populations where two host species are used simultaneously. Host-ant species has an influence on caterpillar size but this varies geographically. Analyses of pupae did not, however, show size differences between M. alcon raised in M. rubra and M. ruginodis nests. 5. The geographical mosaic of host specificity and demography of M. alcon in Denmark probably reflects the co-evolution of M. alcon with two alternative host species. This system therefore provides an interesting opportunity for studying details of the evolution of parasite specificity and the dynamics of host-race formation.

HAL (Le Centre pour la Communication Scientifique Directe), 2007

Insectes Sociaux, Feb 1, 2005

Queens of leafcutter ants (Acromyrmex and Atta) are highly multiply mated, resulting in a potenti... more Queens of leafcutter ants (Acromyrmex and Atta) are highly multiply mated, resulting in a potential queenworker and worker-worker conflict over who should produce the males in the colony. We studied whether this conflict is expressed, by determining the amount of reproductive egglaying by workers in queenright colonies of Acromyrmex echinatior, Acromyrmex octospinosus, Atta cephalotes, and Atta sexdens through ovary dissections. Worker sons are absent or rare in queenright Acromyrmex colonies, but can be produced in orphaned colonies. In Atta, most workers have rudimentary ovaries that never produce eggs, but a few (mostly small and medium workers that form a retinue around the queen) lay many trophic eggs for consumption by the queen. These eggs are large, flaccid, and lacking in yolk compared to queen-laid eggs, and appear to be always inviable. In Acromyrmex, many workers (especially young large workers) lay eggs that are similar in size to queen-laid eggs, but mostly with a reduced amount of yolk. Trophic eggs appear to be an important source of food for larvae in Acromyrmex (especially in Ac. echinatior), but not in Atta. Five (0.8 %) of 616 dissected Ac. echinatior workers but no Ac. octospinosus workers (n = 552), had ready-to-lay reproductive eggs. Old workers in all four species are incapable of laying eggs due to ovary resorption. We conclude that Atta workers are sterile, while Acromyrmex workers display reproductive self-restraint, possibly representing an earlier stage in the evolution towards worker sterility. Worker selfrestraint in Acromyrmex may be maintained by a queen or worker policing mechanism, but individual cost-benefit explanations may also apply.

Journal of Evolutionary Biology, Apr 24, 2012

Wolbachia are renowned as reproductive parasites, but their phenotypic effects in eusocial insect... more Wolbachia are renowned as reproductive parasites, but their phenotypic effects in eusocial insects are not well understood. We used a combination of qrt-PCR, fluorescence in situ hybridization and laser scanning confocal microscopy to evaluate the dynamics of Wolbachia infections in the leaf-cutting ant Acromyrmex octospinosus across developmental stages of sterile workers. We confirm that workers are infected with one or two widespread wsp genotypes of Wolbachia, show that colony prevalence is always 100% and characterize two rare recombinant genotypes. One dominant genotype is always present and most abundant, whereas another only proliferates in adult workers of some colonies and is barely detectable in larvae and pupae. An explanation may be that Wolbachia genotypes compete for host resources in immature stages while adult tissues provide substantially more niche space. Tissuespecific prevalence of the two genotypes differs, with the rarer genotype being over-represented in the adult foregut and thorax muscles. Both genotypes occur extracellularly in the foregut, suggesting an unknown mutualistic function in worker ant nutrition. Both genotypes are also abundant in the faecal fluid of the ants, suggesting that they may have extended functional phenotypes in the fungus garden that the ants manure with their own faeces.

PLOS ONE, Dec 3, 2008

It is unclear why some species become successful invaders whilst others fail, and whether invasiv... more It is unclear why some species become successful invaders whilst others fail, and whether invasive success depends on preadaptations already present in the native range or on characters evolving de-novo after introduction. Ants are among the worst invasive pests, with Lasius neglectus and its rapid spread through Europe and Asia as the most recent example of a pest ant that may become a global problem. Here, we present the first integrated study on behavior, morphology, population genetics, chemical recognition and parasite load of L. neglectus and its non-invasive sister species L. turcicus. We find that L. neglectus expresses the same supercolonial syndrome as other invasive ants, a social system that is characterized by mating without dispersal and large networks of cooperating nests rather than smaller mutually hostile colonies. We conclude that the invasive success of L. neglectus relies on a combination of parasite-release following introduction and preadaptations in mating system, body-size, queen number and recognition efficiency that evolved long before introduction. Our results challenge the notion that supercolonial organization is an inevitable consequence of low genetic variation for chemical recognition cues in small invasive founder populations. We infer that low variation and limited volatility in cuticular hydrocarbon profiles already existed in the native range in combination with low dispersal and a highly viscous population structure. Human transport to relatively disturbed urban areas thus became the decisive factor to induce parasite release, a well established general promoter of invasiveness in non-social animals and plants, but understudied in invasive social insects.

Insectes Sociaux, Mar 13, 2011

The Alcon blue butterfly (Maculinea alcon) parasitizes the nests of several Myrmica ant species. ... more The Alcon blue butterfly (Maculinea alcon) parasitizes the nests of several Myrmica ant species. In Denmark, it uses M. rubra and M. ruginodis, but never M. scabrinodis. To further examine the basis of this specificity and local co-adaptation between host and parasite, the pattern of growth and survival of newly-adopted caterpillars of M. alcon in Myrmica subcolonies was examined in the laboratory. M. alcon caterpillars were collected from three populations differing in their host use, and reared in laboratory nests of all three ant species collected from each M. alcon population. While there were differences in the pattern of growth of caterpillars from different populations during the first few months after adoption, which depended on host ant species and the site from which the ants were collected, there was no evidence of major differences in final size achieved. Survival was, however, much higher in nests of M. rubra than in nests of M. ruginodis and M. scabrinodis, even for caterpillars from a population that is never known to use M. rubra as a host in the field. The caterpillars of M. alcon thus do not show local adaptation in their pattern of growth and survival, but instead show a pattern that may reflect different nestmate recognition abilities of the host ants, related to their sociogenetic organisation. The pattern of observed host ant use in the field seems to result from a combination of differences in local host availability and locally adapted infectivity, modulated by smaller differences in survivorship in the nests of the different host ants.