The temporal stability of plant reproductive features on islands has rarely been tested. Using flowers, fruits/cones and seeds from a well-dated (23 Ma) Miocene Lagerstätte in New Zealand, we show that across 23 families and 30 genera of forest angiosperms and conifers, reproductive features have remained constant for more than 20 Myr. Insect-, wind- and bird-pollinated flowers and wind- and bird-dispersed diaspores all indicate remarkable reproductive niche conservatism, despite widespread environmental and biotic change. In the past 10 Myr, declining temperatures and the absence of low-latitude refugia caused regional extinction of thermophiles, while orogenic processes steepened temperature, precipitation and nutrient gradients, limiting forest niches. Despite these changes, the palaeontological record provides empirical support for evidence from phylogeographical studies of strong niche conservatism within lineages and biomes.
Niche conservatism is a significant constraint on adaptive evolution in organisms and has been advanced as a major influence on speciation and trait development . Integration of phylogenetics with environmental modelling has identified ecological conservatism within both lineages  and biomes . Evidence for niche conservatism comes from similarities between closely related taxa within bioclimatic zones and their shared physiological and morphological traits.
Niche conservatism is the retention of ecological traits over evolutionary time . This is usually inferred by mapping traits onto phylogenies and/or using ancestral state reconstructions to test adaptive shift hypotheses . However, although this approach is informative, it lacks independent evidence for trait consistency or lability over time.
A recent review of niche conservatism suggested that it may break down over long time scales ; a meta-analysis of Holocene speciation and distributional shifts showed conservatism was less dominant across older lineages. Nevertheless, although traits like small leaf size persisted in multiple shrub lineages over 5 Myr of transition from forest to chaparral in California , the rates at which trait conservatism declines within lineages are largely unknown .
Here, we examine features associated with floral structure, pollination and dispersal syndromes in New Zealand, representing an isolated island forest biome with over 20 Myr of environmental change as temperatures declined, mountains arose and environmental gradients steepened . We compare the characteristics of flowers, fruits, cones and seeds from a highly diverse, well-dated Lagerstätte in southern New Zealand with extant relatives .
2. Material and methods
Fossils were recovered from a finely laminated biogenic lake deposit that accumulated in Foulden Maar, a small, deep volcanic crater . Fossils include diatom frustules, insects, fish and plant remains. The flora comprises numerous leaf compressions with cuticle, fruits, seeds, wood, pollen and rare flowers. All material is held in the Geology Museum, University of Otago. The site is dated 23 Ma from radiometric ages from maar-associated basalts .
The comparison between well-preserved fossil and extant genera used well-defined diagnostic characters for assigning the fossils to modern equivalents. These features have been taken from the appropriate taxonomic authorities and are listed in table 1. Many of these assignments have already undergone critical appraisal in other publications (e.g. Fuchsia, Laurelia, Litsea). Once identified, using non-reproductive characters where possible, the pollination and dispersal features of the fossils were compared with data for extant-related New Zealand taxa [12–14,26–29] and lists of floral  and diaspore  reproductive syndrome characteristics.
Floral reproductive parts from 12 mainly thermophilic families are present at the site; in most cases, the identity of these reproductive structures is supported further by fossil leaves and/or pollen. The flowers, from 2 to 20 mm diameter, were probably insect pollinated (Cunoniaceae, Elaeocarpaceae, Lauraceae , Loranthaceae , Meliaceae, Monimiaceae (Hedycarya) , Picrodendraceae, Rutaceae, Sapotaceae ), but some, such as Fuchsia (Onagraceae)  and Alseuosmia (Alseuosmiaceae)  show bird-pollination syndromes, while Malloranga (Euphorbiaceae)  was wind pollinated (table 1).
Nineteen families at the site have fossilized diaspores, ranging from 3 to 50 mm in diameter. Many show animal (bird) dispersal features. These include fleshy fruit/cone (e.g. Araliaceae (Pseudopanax) , Lauraceae , Menispermaceae (Hypserpa) , Moraceae, Myrtaceae (Syzygium), Podocarpaceae (Podocarpus) , Rubiaceae) and arils (e.g. Meliaceae (Dysoxylum) , Elaeocarpaceae (Sloanea), Euphorbiaceae (Malloranga) , Pittosporaceae, Picrodendraceae). The remainder are either wind dispersed (Atherospermataceae (Laurelia) , Bignoniaceae, Casuarinaceae, Cunoniaceae, Proteaceae, Meliaceae), or display no specialized mode of dispersal (Fabaceae, Myrtaceae (Metrosideros), Rutaceae).
Many of these reproductive features show remarkable similarity in appearance with those of extant New Zealand relatives (table 1). For example, strong pollination syndrome conservatism is seen both for generalist insect-pollinated flowers such as Weinmannia (figure 1a,b) and Elaeocarpus (figure 1e,f), specialist Loranthaceae: Elytrantheae (figure 1g,h) and bird-pollinated Alseuosmia (figure 1c,d) and Fuchsia. Similarly, conservatism is apparent in the hairy achenes of Laurelia (figure 1i, j), small bird-dispersed epigynous berries of Pseudopanax (figure 1k,l), large bird-dispersed drupes of Beilschmiedia (figure 1m,n) and capsules of Dysoxylum (figure 1o,p), which contain large, arillate seeds. While preservation limits detailed measurements of many parameters, most of the fossil flowers and diaspores appear remarkably similar to extant relatives (figure 1).
Empirical evidence for reproductive niche conservatism is extremely rare because of the dearth of appropriate sites and fossil material. Foulden Maar is one of the best global pre-Quaternary Lagerstätten examples for such an investigation because it is dated precisely and contains extremely well-preserved fruits and flowers with petals, anthers and often in situ pollen, reproductive organs that are rare globally . Additionally, although all species at Foulden are extinct, most have living relatives in New Zealand, Australia, New Caledonia or South America, allowing explicit comparisons. This contrasts with diverse Eocene-aged Lagerstätten such as Messel and Eckfeld in Germany [31,32] and Laguna del Hunco, Patagonia , which contain fossils phylogenetically more distant from possible living relatives.
Using diagnostic criteria, we show that across 23 families and 30 genera of New Zealand forest plants, including insect-, wind- and bird-pollinated flowers and wind- and bird-dispersed propagules, features have remained relatively constant for more than 20 Myr. This demonstrates remarkable reproductive niche conservatism during a period of widespread environmental change in New Zealand. It is therefore unlikely that these persistent reproductive features were sustained by habitat or environmental filtering. During the Late Cenozoic, New Zealand underwent declining temperatures, renewed tectonic activity and significant reconfiguration of terrestrial habitats with associated cyclical temperature and sea-level changes through the Pleistocene glaciations . However, these processes appear to have eliminated plant taxa primarily on the basis of temperature tolerance , rather than reproductive syndromes .
Changes in pollinator assemblages have caused significant shifts in floral features since the Miocene in other regions. A notable example is the transition from insect to hummingbird pollination in South America where Iochroma (Solanaceae) corolla length increased up to sixfold in strongly bird-pollinated species . By contrast, New Zealand's pollinator assemblage appears to have remained stable, with low diversity of generalist bird pollinators since the Miocene [35,36].
In the New Zealand flora, reproductive conservatism has occurred in lineages with contrasting levels and temporal shifts in richness. For example, Lauraceae and Proteaceae (both over 10 taxa) were highly diverse during the Cenozoic [8,22], but currently have few species (under 3), whereas Rubiaceae and Pittosporaceae remain species rich (both over 20).
Our results indicate that many lineages seem to be highly constrained for reproductive syndromes, this conservatism occurring across all major floral and dispersal types and through periods of substantial environmental change. We find no evidence to support within lineage simplification of floral structures in forest trees and shrubs in New Zealand , unless this had occurred by the mid-Cenozoic.
The Royal Society of New Zealand Marsden fund provided funding.
We thank the Gibson family, Dr Alan Walker and Featherston Resources Ltd for site access.
- Received August 14, 2014.
- Accepted September 23, 2014.
- © 2014 The Author(s) Published by the Royal Society. All rights reserved.