Absence of mammals and the evolution of New Zealand grasses

Abstract

Anthropogenic alteration of biotic distributions and disturbance regimes has dramatically changed the evolutionary context for the differentiation of species traits. Some of the most striking examples in recent centuries have been on islands where flightless birds, which evolved in the absence of mammalian carnivores, have been decimated following the widespread introduction of exotic predators. Until now, no equivalent case has been reported for plants. Here, we make use of robust analytical tools and an exceptionally well-sampled molecular phylogeny to show that a majority of New Zealand danthonioid grasses (Poaceae) may have adapted to the relaxed vertebrate herbivore pressure during the late Cenozoic through the development of a distinctive and unusual habit: abscission of old leaves. This feature occurs in only about 3 per cent of the world's roughly 11,000 grass species and has been empirically shown to increase plant productivity but to reduce protection against mammal grazing. This result suggests that release from a selective pressure can lead to species radiations. This seemingly anachronistic adaptation may represent an overlooked factor contributing to the severe decline in the geographical extent and species diversity of New Zealand's indigenous grasslands following the introduction of herbivorous terrestrial mammals in the 19th century.

Figure 1.

Leaf abscission in grasses. (a) Herbarium specimen of the New Zealand grass Chionochloa rigida, a leaf-abscising species. (b) Detail of fracture zone (inset in (a)) where old leaves are shed.

Figure 2.

Distribution of grass subfamily Danthonioideae. GIS-based map based on 22 025 occurrences from the Global Biodiversity Information Facility (GBIF; www.gbif.org) and 19 372 from various sources. Occurrences coded as New Zealand are marked in red, all others in green.

Figure 3.

Phylogeny of Danthonioideae. Bayesian consensus cladogram showing leaf type and distribution for 270 accessions (representing approx. 81% of all described species; only presence is coded). Relationships were derived from the analysis of 14 425 aligned nucleotide positions from eight plastid and two nuclear DNA sequence regions. See electronic supplementary material, figure S1 for the fully annotated MrBayes consensus tree reporting posterior probabilities for all clades.

Figure 4.

Results from the phylogeny-based analyses of correlation between distribution and leaf type. (a) Likelihood ratio between dependent and independent models, based on ML analyses implemented in BayesTraits [27]; (b) Bayes factor (calculated as twice the difference of the log-harmonic mean between dependent and independent analyses) plotted against iteration in the reversible-jump MCMC analysis in BayesTraits [27]. The analysis stabilizes after an initial burn-in phase. The dashed lines indicate significance levels, under which there is ‘very strong evidence’ for correlation [30].