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Reproductive niche conservatism in the isolated New Zealand flora over 23 million years John G. Conran, William G. Lee, Daphne E. Lee, Jennifer M. Bannister and Uwe Kaulfuss Biol. Lett. 2014 10, 20140647, published 15 October 2014

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Research Cite this article: Conran JG, Lee WG, Lee DE, Bannister JM, Kaulfuss U. 2014 Reproductive niche conservatism in the isolated New Zealand flora over 23 million years. Biol. Lett. 10: 20140647. http://dx.doi.org/10.1098/rsbl.2014.0647

Received: 14 August 2014 Accepted: 23 September 2014

Subject Areas: ecology, evolution, palaeontology Keywords: niche conservatism, islands, reproduction, flowers, fruits, fossils

Reproductive niche conservatism in the isolated New Zealand flora over 23 million years John G. Conran1, William G. Lee2,3, Daphne E. Lee4, Jennifer M. Bannister5 and Uwe Kaulfuss4 1

ACEBB & SGC, School of Earth and Environmental Sciences, DX 650-312, The University of Adelaide, Adelaide, South Australia 5005, Australia 2 Landcare Research, Private Bag 1930, Dunedin 9054, New Zealand 3 School of Biological Sciences, University of Auckland, Private Bag 92019, Auckland 1010, New Zealand 4 Department of Geology, and 5Department of Botany, University of Otago, PO Box 56, Dunedin 9054, New Zealand JGC, 0000-0003-2268-2703 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 Lagersta¨tte 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.

1. Introduction Author for correspondence: John G. Conran e-mail: [email protected]

Niche conservatism is a significant constraint on adaptive evolution in organisms and has been advanced as a major influence on speciation and trait development [1]. Integration of phylogenetics with environmental modelling has identified ecological conservatism within both lineages [2] and biomes [3]. 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 [4]. This is usually inferred by mapping traits onto phylogenies and/or using ancestral state reconstructions to test adaptive shift hypotheses [5]. 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 [6]; 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 [5], the rates at which trait conservatism declines within lineages are largely unknown [6]. 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 [7]. We compare

& 2014 The Author(s) Published by the Royal Society. All rights reserved.

pollen leaves

fruits

flowers with in situ pollen; fruit

flowers; fruits (Sloanea only)

flowers with in situ pollen; fruits; seeds fruits; ?seeds

flowers; fruits; seeds

Casuarinaceae (?Casuarina) [18]

Cunoniaceae (Weinmannia) [17]

Elaeocarpaceae (Elaeocarpus and Sloanea) [17,18,20]

Euphorbiaceae (Malloranga) [21]

flower with in situ pollen

flower with in situ pollen; fruits

endocarps

Loranthaceae [17]

Meliaceae (Dysoxylum and others) [18]

Menispermaceae (Hypserpa) [23]

Fabaceae subfam. Caesalpinioideae [8,18] Lauraceae (?Beilschmiedia, ?Cryptocarya, ?Litsea) [22]

—

winged seeds

leaves

leaves, pollen

pollen; ?leaves

leaves; pollen

leaves

leaves; pollen

pollen

leaves, pollen

fruits

leaves; pollen

umbels of flowers and fruits

Atherospermataceae (Laurelia) [19] Bignoniaceae [18]

—

flower

Alseuosmiaceae (Alseuosmia) [17] Araliaceae (Pseudopanax) [18]

for occurrence

other evidence

at Foulden

Hypserpa (AU, NC, NG)

Dysoxylum*

Alepis*, †Trilepidea

Beilschmiedia*, Cryptocarya (OT), Litsea*

Caesalpinioid legumes (PT)

Mallotus, Macaranga (PT)

Elaeocarpus*, Sloanea (PT)

NG, AS) Casuarina (AU, NC), Allocasuarina (AU), Gymnostoma (AU, NC, NG, AS) Weinmannia*

?Tecomanthe*, ?Deplanchea (AU, NC,

Laurelia*

Pseudopanax*

Alseuosmia*

modern relatives

sepals and petals 4 –5; staminal tube cylindrical, toothed at mouth; anthers 8 –10, included in tube; disk tubular; capsule loculicidally dehiscent; seeds endocarp bony, curved, rugulose with radial transverse ridges; condyle with two lateral externally aperturate cavities

perianth of four reflexed petaloid tepals; stamens 4; stigma 1

flowers small, one to clustered, occasionally involucrate; calyx tube short, sometimes, lobes or teeth 4–6; fruit a oneseeded berry, pome or drupe

five valved, smooth to spinose hairy flowers 2–3 mm diam.; stamens numerous; capsules three locular, one seeded, hairy; seeds globular fruit a legume, mostly dry, dehiscent or indehiscent

sepals 4– 5, united basally, imbricate; petals 4–5; stamens 8– 10; ovary two locular; capsules two valved, septicidally dehiscent petals 4– 5; stamens numerous; anthers linear, +awned, opening by terminal pores or slits; fruits 3 –5 cm, two to

fruit woody, oval, cone like; carpels numerous, one seeded

corolla long funnelform, five lobed. Stamens 5, inserted near throat (exserted in dry flowers) umbellate; petals 5; styles shortly connate; fruit + fleshy, five locular achenes with long, plumose styles, enclosed in enlarged receptacle seed wing transparent, very thin; embryo tear-drop shaped

diagnostic features shared with modern relatives

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taxon

(Continued.)

dish bowl (H): small insect (P)/ avichory (D)

bell flowers, explosive pollen (H): birds, bees, wasps (P)/avichory (D) dish bowl (H): small insect (P)/ avichory (D)

(H); hydrochory, zoochory or ballistochory (D) dish bowl (H): small insect (P)/ avichory (D)

brush (U): wind (P)/avichory (D)

bell flowers (H): small insect (P)/ avichory (D)

brush (H): small insect (P)/ anemochory (D)

(U) anemochory (D)

(H) anemochory (D)

dish bowl (U): small insect (P)/ avichory (D) (U/H) anemochory (P/D)

bell flower (H): bird, moth (P)

reproductive syndromes

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reproductive organs preserved

Table 1. Plant families and genera with macrofossil material at Foulden Maar based on reproductive structures (flower, fruit and seed), supporting evidence for identification to extant relatives (Adapted from [10,11]), and reproductive syndrome data [12 – 16]. Voucher specimens of the fossils are housed at the University of Otago Geology Museum (OU). U, unisexual; H, hermaphrodite; P, pollination and D, dispersal. AU¼Australia, NC¼New Caledonia, NG¼New Guinea, AS¼South-east Asia, OT¼Old World tropics, PT¼Pantropical

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2

pollen

fruits; seeds

flower and anther mass with in situ pollen male flowers with in situ pollen; female flowers; fruits male flowers with in situ pollen; female flowers; fruits

Moraceae (?Streblus) [18]

Myrtaceae (Metrosideros and Syzygium) [18] Onagraceae (Fuchsia) [24]

flower bud with in situ pollen

Sapotaceae (Planchonella) [17]

*Present in modern New Zealand; †recently extinct.

flowers with in situ pollen; bud; ?seeds

Rutaceae (?Melicope, †Fouldenia, ?Neoschmidia) [17] ?leaves, pollen

leaves, possible pollen

pollen

leaves; pollen

winged seed

infructescence

leaves; pollen

cone with seeds

Planchonella*

Melicope*, Neoschmidia (NC); affinities of Fouldenia uncertain

Coprosma*

Stenocarpus (AU, NC, NG), Alloxylon (AU, NG)

Podocarpus*

Pittosporum*

Whyanbeelia (AU)

pollen; ?leaves

–

Scagea (NC)

Fuchsia*

Metrosideros*, Syzygium*

Streblus*

Hedycarya*

modern relatives

pollen; ?leaves

pollen

fruit

?Rubiaceae (Coprosma) [18]

?Pittosporaceae (Pittosporum) [18] Podocarpaceae (Podocarpus) [18,25] ?Proteaceae (?Stenocarpus or ?Alloxylon) [18]

Picrodendraceae (?Scagea) [17,18] Picrodendraceae (?Whyanbeelia) [17,18]

leaves; pollen

possible infructescence

Monimiaceae (Hedycarya) [17]

leaves

flowers with in situ pollen; fruits

taxon

other evidence for occurrence

fruits +globose drupes, sessile, sometimes in decussate pairs along infructescence stalk Melicope: flowers 4-merous, petals with inflexed apices Neoschmidia flowers actinomorphic, petals 5, thick, one nerved, ovate-elliptic; stamens 10, anthers glabrous Flower buds ovoid-elliptical, pedicellate, densely hairy with prominent hair bases

styles 3–4 mm; disk glands prominent; fruits globular, +20 mm, mericarps separating at maturity fruit a two- to three-segmented loculicidal capsule, segments rounded, spreading receptacle fleshy; epimatium connate with inverted ovule, concrescent with integument; seed nut-like Seeds flat, with a narrow, oblong, terminal wing and large seed body

receptacle adnate to inferior ovary; fruit a one-seeded ‘berry’ (Syzygium) or many-seeded loculicidal capsule (Metrosideros) floral tube tubular; sepals 4; petals minute or 0; stamens 8, in two whorls, exserted; anthers dorsifixed staminate flower tepals concave, three outer and three inner; stamens (4–)6; pistillode usually present male flowers short pedicellate, tepals 1–1.5 mm, stamens 50 –55; female flowers long pedicellate, tepals 3– 4 mm,

dioecious, flowers cup shaped, male perianth 5 –10 partite, spreading; stamens numerous, anthers flat, +sessile; drupes several on receptacle unisexual flowers in spikes with distinctive flattened scales; fruit a one-seeded drupe

diagnostic features shared with modern relatives

Biol. Lett. 10: 20140647

reproductive organs preserved at Foulden

bell (H): bees (P)/ avichory (D)

dish bowl (H/U): small insect (P)/ avichory (D)

brush (H): wind (P)/ avichory (D)

bell (H): bird (P)/anemochory (D)

wind (U); avichory (D)

bell (H): bees (P)/avichory (D)

dish bowl (U): small insect (P)/ avichory (D)

dish bowl (U): small insect (P)

inflorescence (H): bird, insect (P)/ avichory (D) bell (H/U): bird (P)/avichory (D)

brush (U): wind (P)/avichory (D)

dish bowl (U): small insect (P)/ avichory (D)

reproductive syndromes

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Table 1. (Continued.)

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3

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(b)

(c)

(d)

(e)

(f)

(g)

(h)

(i)

( j)

(k)

(l)

(m)

(n)

(o)

(p)

4

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(a)

the characteristics of flowers, fruits, cones and seeds from a highly diverse, well-dated Lagersta¨tte in southern New Zealand with extant relatives [8].

2. Material and methods Fossils were recovered from a finely laminated biogenic lake deposit that accumulated in Foulden Maar, a small, deep volcanic crater [9].

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 [9]. 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

Biol. Lett. 10: 20140647

Figure 1. Comparison of fossil and modern New Zealand flowers, fruits and seeds. (a) Fossil and (b) living Cunoniaceae (Weinmannia) flowers (generalist insect pollination). (c) Fossil and (d ) living Alseuosmiaceae (Alseuosmia) flowers (bird pollination). (e) Fossil and ( f ) living Elaeocarpaceae (Elaeocarpus) flowers (generalist insect pollination). (g) Fossil (tribe Elytrantheae) and (h) living Loranthaceae (Alepis) flowers (specialist insect pollination). (i) Fossil and ( j ) living Atherospermataceae (Laurelia) achene (wind dispersal). (k) Fossil and (l ) living Araliaceae (Pseudopanax) berries (small bird dispersal). (m) Fossil and (n) living Lauraceae (Beilschmiedia) berries (large bird dispersal). (o) Fossil and ( p) living Meliaceae (Dysoxylum) capsules (arillate seed dispersal). Scale bars: a, b, i, j ¼ 2 mm, c– h, k, l ¼ 5 mm, m – p ¼ 10 mm. (Online version in colour.)

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3. Results

4. Discussion 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

Acknowledgements. We thank the Gibson family, Dr Alan Walker and Featherston Resources Ltd for site access.

Funding statement. The Royal Society of New Zealand Marsden fund provided funding.

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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 [22], Loranthaceae [17], Meliaceae, Monimiaceae (Hedycarya) [17], Picrodendraceae, Rutaceae, Sapotaceae [17]), but some, such as Fuchsia (Onagraceae) [24] and Alseuosmia (Alseuosmiaceae) [17] show bird-pollination syndromes, while Malloranga (Euphorbiaceae) [21] 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) [18], Lauraceae [22], Menispermaceae (Hypserpa) [23], Moraceae, Myrtaceae (Syzygium), Podocarpaceae (Podocarpus) [25], Rubiaceae) and arils (e.g. Meliaceae (Dysoxylum) [18], Elaeocarpaceae (Sloanea), Euphorbiaceae (Malloranga) [21], Pittosporaceae, Picrodendraceae). The remainder are either wind dispersed (Atherospermataceae (Laurelia) [19], 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).

pre-Quaternary Lagersta¨tten 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 [30]. 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 Lagersta¨tten such as Messel and Eckfeld in Germany [31,32] and Laguna del Hunco, Patagonia [33], 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-, windand 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 [7]. However, these processes appear to have eliminated plant taxa primarily on the basis of temperature tolerance [7], rather than reproductive syndromes [28]. 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 [34]. 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 [28], unless this had occurred by the mid-Cenozoic.

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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 [15] and diaspore [16] reproductive syndrome characteristics.

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