Evolutionary consequences of shifts to bird-pollination in the Australian pea-flowered legumes (Mirbelieae and Bossiaeeae)
© Toon et al.; licensee BioMed Central Ltd. 2014
Received: 6 September 2013
Accepted: 19 February 2014
Published: 7 March 2014
Interactions with pollinators are proposed to be one of the major drivers of diversity in angiosperms. Specialised interactions with pollinators can lead to specialised floral traits, which collectively are known as a pollination syndrome. While it is thought that specialisation to a pollinator can lead to either an increase in diversity or in some cases a dead end, it is not well understood how transitions among specialised pollinators contribute to changes in diversity. Here, we use evolutionary trait reconstruction of bee-pollination and bird-pollination syndromes in Australian egg-and-bacon peas (Mirbelieae and Bossiaeeae) to test whether transitions between pollination syndromes is correlated with changes in species diversity. We also test for directionality in transitions that might be caused by selection by pollinators or by an evolutionary ratchet in which reversals to the original pollination syndrome are not possible.
Trait reconstructions of Australian egg-and-bacon peas suggest that bee-pollination syndrome is the ancestral form and that there has been replicated evolution of bird-pollination syndromes. Reconstructions indicate potential reversals from bird- to bee-pollination syndromes but this is not consistent with morphology. Species diversity of bird-pollination syndrome clades is lower than that of their bee-pollination syndrome sisters.
We estimated the earliest transitions from bee- to bird-pollination syndrome occurred between 30.8 Ma and 10.4 Ma. Geographical structuring of pollination syndromes was found; there were fewer bird-pollination species in the Australian southeast temperate region compared to other regions of Australia.
A consistent decrease in diversification rate coincident with switches to bird pollination might be explained if greater dispersal by bird pollinators results in higher levels of connectivity among populations and reduced chances of allopatric speciation.
The earliest transitions overlap with the early diversification of Australian honeyeaters – the major lineage of pollinating birds in Australia. Our findings are consistent with the idea that environment and availability of pollinators are important in the evolution of pollination syndromes. Changes in flower traits as a result of transitions to bird-pollination syndrome might also limit reversals to a bee-pollination syndrome.
KeywordsPollination syndrome Adaptive radiation Ancestral state reconstruction Diversification
The extraordinary radiation of flowering plants (angiosperms) accounts for about 91% of all plant species and forms the foundations of terrestrial biodiversity [1, 2]. This expansive evolution of species and morphological diversity has been attributed, at least in part, to interactions with animals [3, 4] – particularly changes in specialist pollinators that might drive diversification [5–7]. There is good evidence that shifts between specialized pollinators are correlated with increased diversification in some angiosperm groups and decreases in others [8, 9].
Is pollination syndrome correlated with species diversity? If pollinators are influencing angiosperm diversification, there might be observable differences in diversity after shifts in pollinator.
Are all shifts equally likely? It would be expected that, if pollinator use is correlated with environment or if there is an evolutionary ratchet mechanism, there would be asymmetry in the directions of pollinator shifts.
We sampled about half of the 700 known species of Mirbelieae and Bossiaeeae (Fabaceae, Australian egg-and-bacon peas), which are comprised of major endemic Australian pea genera such as Daviesia, Bossiaea, Pultenaea, Mirbelia and Gastrolobium. Trees were rooted with outgroups that included the likely sister group (Hypocalyptus), and other taxa sampled from across the legumes using Wojciechowski et al. (2004)  as a guide to relationships. Sequences of two cpDNA loci (ndhF and trnL-trnF) and one nrDNA locus (ITS1, 5.8S and ITS2) were obtained from our previous studies ( and references cited therein). DNA sequences were edited using Sequencher v4.5 (GeneCodes) and aligned manually in Se-Al v2.0a11 . Parts of the ITS and trnL-trnF sequences that were not confidently aligned across the more distantly related terminals were offset or omitted. Ambiguity in aligning trnL-trnF and ITS prevented the use of outgroups more distantly related than Baphia.
Phylogenies were estimated for each locus using maximum likelihood (ML) in GARLI v0.951  and a Bayesian MCMC search using MrBayes v3.1.2 . All phylogenetic analyses incorporated a GTR + I + G model. As the resulting topologies and branch lengths showed little difference between the two search methods, all subsequent analyses used the GARLI trees with the best likelihood scores. The trnL-trnF and ndhF data showed no supported differences in resolution and were combined into a single cpDNA partition for comparative analyses. Other specifics of analyses were as per Crisp and Cook .
Phylograms were transformed into chronograms, in which branch lengths were proportional to time, using penalized likelihood (PL) in r8s v1.71  with smoothing parameters optimised by fossil-based cross validation. To estimate ages of nodes, several primary (fossil-based) and secondary calibration points were used, as described previously . We used the dated phylogenies to infer the timing of the earliest transitions between pollination syndromes. Confidence intervals around stem nodes of bird-pollination syndrome clades (crown node ages represent the latest possible transition time) were estimated from the ITS data and from the combined cpDNA data using 100 ML bootstrap trees with the ‘profile’ function in r8s.
Transitions between pollination syndromes
Ancestral states for the root and internal nodes were inferred from each phylogeny using parsimony-based models as implemented in Mesquite version 2.74 : equal-weighted parsimony and Dollo parsimony (bird, once gained from bee, is irreversible). The “Dollo” model is based on the arguments that, once lost, a complex trait cannot revert to exactly the same form it was before the change [36, 37]. Pollination syndrome may satisfy the criterion of a complex trait because flowers of different syndromes differ in multiple, integrative floral attributes, including colour, shape, nectar and orientation . If evolution of floral morphology underlying a bird-pollination syndrome involves changes in multiple pathways, it might be expected that changes back to a bee-pollination syndrome might be difficult or, if it does occur, results in a morphology that is somewhat different from the ancestral bee-pollinated floral morphology.
Differences in diversity
If shifts in pollination syndrome have contributed to the diversity of angiosperms, we might expect there to be observable differences in species diversity of clades exhibiting different pollination syndromes. Sister-clade comparisons are a good way of testing for species-richness differences if a sufficient number of pairs are available to provide power to the test. Sister clades share a single common ancestor and so any differences in species diversity must have arisen since their divergence from that ancestor. We tested whether there was a difference in species richness between clades with bird- and bee-pollination syndrome using a Wilcoxon signed-rank test of sister clades as implemented in GraphPad Prism 5.03, GraphPad Software, San Diego California USA, www.graphpad.com. Given that there were slight differences in topologies among trees derived from the different DNA regions, we conducted the sister-taxon comparisons separately using ML trees from both ITS and combined cpDNA. One sister pair of bird-bee-pollination syndrome was removed from the ITS analysis because of uncertain phylogenetic resolution. There was insufficient phylogenetic resolution to identify the sister to the bird-pollination syndrome clade (i.e., it was part of a polytomy) in Gastrolobium in both gene trees, so we combined the unresolved bee-pollination syndrome species into a single clade. Combining these clades did not bias the result because the total species diversity of the combined bee-pollination syndrome clades was less than that of the bird-pollination syndrome clade – our approach was conservative. To complement the sister-pair comparisons, we used the BiSSE approach  available in Mesquite v2.74 (with the Goldberg correction module, ) to test the null hypothesis that diversification rates remained constant through inferred transition events, i.e., that there was no difference in diversification rates of bee- and bird-pollination syndrome clades. We compared the models using Akaike information criterion (AIC) following Burnham , where the model with the lower score is a better fit.
Geographic distribution of pollination syndromes
If different pollination syndromes are favoured under different ecological conditions, we might expect them to be represented differently in each major habitat. We tested whether there was geographic variation in the proportion of bird- and bee-pollination syndrome species richness as a proxy for an external ecological driver. We categorised all described species of Mirbelieae and Bossiaeeae as occurring in one or more of four biomes based on distribution data from Australia’s Virtual Herbarium (http://chah.gov.au/avh/index.jsp, accessed 11 Nov 2011) and regions described in [41, 42]: southeast temperate, southwest temperate, central (arid), and tropical (monsoon tropics). We used a Chi-squared test to determine whether there was a difference in the proportion of bird-pollination syndrome species occurring in these regions.
We compared diversity of sister clades differing in pollination syndrome and found that clades of species with bird-pollination syndrome had fewer species than their sister clade with bee-pollination syndrome (Wilcoxon signed-rank tests: combined cpDNA: n = 11, Z = -2.073, P = 0.038; ITS: n = 11, Z = -2.014, P = 0.044). The BiSSE model, which accounts for interaction between trait states and diversification rates, marginally supported the state-independent maximum likelihood (ML) models over state-dependent models (delta AIC = 3.96), although both models are still favoured where delta AIC < 4 .
Shifts in pollination syndrome
Number of transitions between bee- and bird-pollination syndromes inferred from maximum parsimony (MP) reconstruction methods using the ITS and cpDNA phylogeny
Bee to bird
Bird to bee (reversals)
MP (equal weighted) - MPR1
MP (equal weighted) - MPR2
MP (equal weighted)
Geographic distribution of pollination syndromes
There are proportionally fewer bird-pollination syndrome species of egg-and-bacon peas in the Australian southeast temperate region (SET) (about 1%) than any other region (Chi-squared = 15.108, df = 3, P = 0.0017), and no significant difference between proportions in the southwest temperate (5.9%), tropical (9.3%) and central (10.5%) regions (Chi-squared = 2.781, df = 2, P = 0.249).
Pea flowers of the subfamily of legumes classified as Faboideae (or Papilionoideae) arose about 58 Ma  and are thought to have evolved as a specialisation to pollination by bees . Our reconstruction of a bee-pollination syndrome as ancestral for the Australian egg-and-bacon peas is consistent with it being the ancestral syndrome for the entire subfamily. The main bird pollinators of Australian egg-and-bacon peas, the honeyeaters (Meliphagidae), probably radiated between 15.9-29.4 Ma . The earliest transitions to bird-pollination syndrome, which we estimated to have occurred ca. 10.4-30.8 Ma (cpDNA) and 7.6-29.6 Ma (ITS), mostly overlap with the radiation of honeyeaters. Thus, our results are consistent with this pollination syndrome being dependent on the availability of potential pollinators: bees of several families were present in Australia before the diversification of honeyeaters (e.g., [46, 47]), and it appears that egg-and-bacon peas only switched to bird-pollination syndromes once the honeyeaters were present to exert selection pressure on flower morphology. The honeyeaters have a visual system that responds well to the red wavelengths , and multiple lineages of Australian plants, such as Proteaceae , appear to have developed floral syndromes that are coloured for the tetrachromic vision of honeyeaters after this group radiated .
Similarly to reports for some plants outside Australia (e.g., [51, 52]), we found that lineages of the Australian egg-and-bacon peas exhibiting a bird-pollination syndrome have fewer species than their sister clades of bee-pollination syndrome species. Differences in species diversity are explained by changes in diversification rate, that is, in the rates of speciation and/or extinction. Pollination syndromes could directly influence either rate (speciation or extinction) by affecting genetic connectivity across a species’ range over time . Different pollinators move pollen across different distances, thus affecting genetic connectivity across a species range (eg., [54, 55]). Australian honeyeaters have been found to distribute pollen over distances of 103-104 metres whereas bees typically do so over 102 metres [56–58], and bees transfer pollen between flowers less efficiently than birds . Lower levels of pollen movement could lead to greater spatial genetic structure and increase the chance of speciation via allopatric speciation in bee-pollinated taxa compared to bird-pollinated taxa. The corollary of this is that bird-pollinated taxa should be subject to lower levels of differentiation in allopatry.
Directional bias in transitions in pollination syndrome
The floral morphology that suits pollination by birds might have resulted in sexual parts oriented in such a way that bees do not transfer pollen between flowers, and thus do not exert selection pressure on bird-pollination syndrome flowers. That is, the system represents an evolutionary ratchet mechanism where, once floral morphology has diverged sufficiently, reversions to the previous state are rare.
Although all reconstructions favoured at least one reversal from bird-pollination syndrome to bee-pollination syndrome, a Dollo model (no reversals) required only one or two additional switches in pollination syndrome (Table 1). Determining which reconstruction is most accurate cannot be determined from phylogenies alone (e.g., [59, 60]) and additional information is required to test hypothesised pathways. Under a scenario of replicated evolution of a trait (here bird-pollination syndrome) it is expected that, in most cases, the trait will have evolved in slightly different ways because the lineages are independent, although they might be closely related. This is evident in parallel transitions to bird-pollination syndrome in egg-and-bacon peas. There are some commonalities, such as enlarged and/or red tubular corollas, but there are also lineage-specific differences, as expected. For example, G. rubrum and G. bracteolosum have a reduced standard, enlarged keel and are pendulous, whereas some others (G. leakeanum, G. mondurup and G. vestitum) have a flower shape more similar to a typical bee-pollination syndrome but are resupinate (turned upside down) and much larger (Figure 5). Others, such as G. melanopetalum, G. sericeum and G. modestum, have cream or black flowers that are inflated at the base, with a small keel and canaliculate (longitudinally grooved) standard.
An alternative explanation to the bias in direction of pollination syndrome transitions might be that current environmental conditions favour bird pollination over bee pollination, and thus there is little selection favouring reversals. Orians and Milewski  postulated that Australia has more vertebrate-pollinated species than other continents because it has poor soils and ample sunshine. Under such conditions and with sufficient water, plants are able to produce excess carbohydrates and thus make copious quantities of nectar, which attracts large vertebrates . The nectar produced on nutrient poor soil might be low in proteins , however, unlike insect-pollinators, vertebrates readily acquire proteins from other sources in their diet such as insects . Our findings are partly consistent with this idea because we found greater proportions of bird-pollination syndrome egg-and-bacon peas in regions with poorest soils (southwest temperate, central and tropical Australia) compared with the more fertile southeast temperate region. However, the ability to make copious nectar cannot explain the transition to a bird-pollination syndrome, only that it is possible. Other ecological factors that favour bird over bee pollination must be present. For example, differences in abundance of pollinators across the landscape might drive the initial divergence needed for speciation [5, 6], and classic studies on Mimulus  support this as a likely mechanism. Most Australian honeyeaters feed also on insects and are not limited to nectar , so they can persist in areas and through seasons when bees are absent. Pollinator abundance might also be influenced by the presence of other species of flowering plants. Coexistence of peas in a community with a high abundance of bird-pollinated taxa, such as in southwest Western Australia , might promote reproductive success in peas that switch to bird-pollination by increasing visitation of pollinators and providing shelter and nesting for birds, as suggested for banksias and eucalypts by He et al. .
The Australian egg-and-bacon peas exhibit replicated evolution of bird-pollination syndromes, with little evidence that there have been switches back to an ancestral-type bee-pollination syndrome. Our reconstructions inferred that a shift in pollinator has repeatedly led to a decrease in diversification rate, with bird-pollination syndrome clades less species rich than their bee-pollination syndrome sisters. This might be explained if greater dispersal of bird-pollinators results in higher levels of connectivity and decreases the chance of allopatric speciation in bird-pollinated species. Further studies comparing gene flow and population structure will contribute towards an understanding of how different pollination specialisations have contributed to the diversification of angiosperms.
Availability of supporting data
Additional file 1: Figure S1.
Additional file 2: Figure S2.
Akaike information criterion
Southeast temperate region
Southwest temperate region.
We thank David Morris for some DNA sequencing and Emma Goldberg for supplying a script for setting root states in Mesquite. Funding was provided by the Australian Research Council (grant number: DP0985473). We thank the Papers in the Pub and Coopers & Cladistics discussion groups and the Cook and Crisp lab groups, for valuable discussion on ancestral state reconstruction and modelling of tree.
- Paton AJ, Brummitt N, Govaerts R, Harman K, Hinchcliffe S, Allkin B, Lughadha EN: Towards target 1 of the global strategy for plant conservation: a working list of all known plant species-progress and prospects. Taxon. 2008, 57 (4): 1371-1371.Google Scholar
- The plant list. Vol. Version 1. 2010, http://www.theplantlist.org/ (accessed 2nd May 2013)
- Crepet WL, Niklas KJ: Darwin’s second “abominable mystery”: why are there so many angiosperm species?. Am J Bot. 2009, 96 (1): 366-381. 10.3732/ajb.0800126.PubMedView ArticleGoogle Scholar
- de Saporta G, Marion AF: L’évolution du règne végétal. Les Phanérogames. 1885, Saint Germain, France: Ancienne Librairie Germer BaillièreGoogle Scholar
- Grant V: Pollination systems as isolating mechanisms in angiosperms. Evolution. 1949, 3 (1): 82-97. 10.2307/2405454.PubMedView ArticleGoogle Scholar
- Stebbins GL: Adaptive radiation of reproductive characteristics in angiosperms. I. Pollination mechanisms. Annu Rev Ecol Syst. 1970, 1: 307-326. 10.1146/annurev.es.01.110170.001515.View ArticleGoogle Scholar
- Johnson SD: The pollination niche and its role in the diversification and maintenance of the southern African flora. Philos Trans R Soc Lond B Biol Sci. 2010, 365 (1539): 499-516. 10.1098/rstb.2009.0243.PubMedPubMed CentralView ArticleGoogle Scholar
- Kay KM, Sargent RD: The role of animal pollination in plant speciation: integrating ecology, geography, and genetics. Annu Rev Ecol Evol Syst. 40: 637-656.
- Smith SD: Using phylogenetics to detect pollinator-mediated floral evolution. New Phytol. 2010, 188 (2): 354-363. 10.1111/j.1469-8137.2010.03292.x.PubMed CentralView ArticleGoogle Scholar
- Ollerton J, Winfree R, Tarrant S: How many flowering plants are pollinated by animals?. Oikos. 2011, 120 (3): 321-326. 10.1111/j.1600-0706.2010.18644.x.View ArticleGoogle Scholar
- Gegear RJ, Burns JG: The birds, the bees, and the virtual flowers: can pollinator behavior drive ecological speciation in flowering plants?. Am Nat. 2007, 170 (4): 551-566. 10.1086/521230.PubMedView ArticleGoogle Scholar
- Fenster CB, Armbruster WS, Wilson P, Dudash MR, Thomson JD: Pollination syndromes and floral specialization. Annu Rev Ecol Evol Syst. 2004, 35 (1): 375-403. 10.1146/annurev.ecolsys.34.011802.132347.View ArticleGoogle Scholar
- Proctor M, Yeo P, Lack A: The Natural History of Pollination. 1996, London: Harper Collins PublishersGoogle Scholar
- Peitsch D, Fietz A, Hertel H, Desouza J, Ventura DF, Menzel R: The spectral input systems of hymenopteran insects and their receptor-based color-vision. J Comp Physiol A. 1992, 170 (1): 23-40.PubMedView ArticleGoogle Scholar
- Briscoe AD, Chittka L: The evolution of color vision in insects. Annu Rev Entomol. 2001, 46: 471-510. 10.1146/annurev.ento.46.1.471.PubMedView ArticleGoogle Scholar
- Gross CL: Floral traits and pollinator constancy: foraging by native bees among three sympatric legumes. Aust J Ecol. 1992, 17: 67-74. 10.1111/j.1442-9993.1992.tb00781.x.View ArticleGoogle Scholar
- Cresswell JE: Stabilizing selection and the structural variability of flowers within species. Ann Bot. 1998, 81 (4): 463-473. 10.1006/anbo.1998.0594.View ArticleGoogle Scholar
- Whittall JB, Hodges SA: Pollinator shifts drive increasingly long nectar spurs in columbine flowers. Nature. 2007, 447 (7145): 706-712. 10.1038/nature05857.PubMedView ArticleGoogle Scholar
- Thomson JD, Wilson P: Explaining evolutionary shifts between bee and hummingbird pollination: convergence, divergence, and directionality. Int J Plant Sci. 2008, 169 (1): 23-38. 10.1086/523361.View ArticleGoogle Scholar
- Tripp EA, Manos PS: Is floral specialization an evolutionary dead-end? Pollination system transitions in Ruellia (Acanthaceae). Evolution. 2008, 62 (7): 1712-1737. 10.1111/j.1558-5646.2008.00398.x.PubMedView ArticleGoogle Scholar
- Schemske DW, Bradshaw HD: Pollinator preference and the evolution of floral traits in monkeyflowers (Mimulus). Proc Natl Acad Sci USA. 1999, 96 (21): 11910-11915. 10.1073/pnas.96.21.11910.PubMedPubMed CentralView ArticleGoogle Scholar
- Brown EM, Burbidge AH, Dell J, Edinger D, Hopper SD, Wills RT: Pollination in Western Australia: A Database of Animals Visiting Flowers. 1997, Perth: Western Australian Naturalists’ ClubGoogle Scholar
- Hingston AB, Mc Quillan PB: Are pollination syndromes useful predictors of floral visitors in Tasmania?. Austral Ecol. 2000, 25 (6): 600-609. 10.1111/j.1442-9993.2000.tb00065.x.View ArticleGoogle Scholar
- Keighery GJ: Bird pollination in south Western Australia - a checklist. Plant Syst Evol. 1980, 135 (3–4): 171-176.View ArticleGoogle Scholar
- Keighery GJ: Bird-Pollinated Plants in Western Australia. Pollination and Evolution. Edited by: Armstrong JA, Powell JM, Richards AJ. 1982, Sydney: Royal Botanic Gardens, 77-89.Google Scholar
- Keighery GJ: Pollination of Jansonia formosa Kipp. ex Lindl. (Papilionaceae). West Aust Nat. 1984, 16: 21-Google Scholar
- Crisp MD: Evolution of bird-pollination in some Australian legumes (Fabaceae). Linn Soc Symp Ser. 1994, 17: 281-309.Google Scholar
- Crisp MD: Convergent Evolution of Bird Pollination in Western Australian Fabaceae and its Taxonomic Implications. Gondwanan Heritage: Past, Present and Future of the Western Australian Biota. Edited by: Hopper SD, Chappill JA, Harvey MS, George AS. 1996, Chipping Norton, NSW: Surrey Beatty & Sons, 179-186.Google Scholar
- Wojciechowski MF, Lavin M, Sanderson MJ: A phylogeny of legumes (Leguminosae) based on analysis of the plastid matKgene resolves many well-supported subclades within the family. Am J Bot. 2004, 91: 1846-1862. 10.3732/ajb.91.11.1846.PubMedView ArticleGoogle Scholar
- Crisp MD, Cook LG: Explosive radiation or cryptic mass extinction? Interpreting signatures in molecular phylogenies. Evolution. 2009, 63 (9): 2257-2265. 10.1111/j.1558-5646.2009.00728.x.PubMedView ArticleGoogle Scholar
- Rambaut A: Se-Al: Sequence Alignment Editor. 1996, University of Oxford, Department of Zoology, Available at http://tree.bio.ed.ac.uk/Google Scholar
- Zwickl DJ: Genetic Algorithm Approaches for the Phylogenetic Analysis Large Biological Sequence Datasets Under the Maximum Likelihood Criterion. 2006, Dissertation: Ph.DGoogle Scholar
- Ronquist F, Huelsenbeck JP: MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics. 2003, 19 (12): 1572-1574. 10.1093/bioinformatics/btg180.PubMedView ArticleGoogle Scholar
- Sanderson MJ: r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics. 2003, 19 (2): 301-302. 10.1093/bioinformatics/19.2.301.PubMedView ArticleGoogle Scholar
- Maddison WP, Maddison DR: Mesquite: a modular system for evolutionary analysis. 2010, Version 2.73 http://mesquiteproject.orgGoogle Scholar
- Dollo L: Les lois de l’évolution. Bulletin de la Société Belge de Géologie de Paléontologie et d’Hydrologie. 1893, 7: 164-166.Google Scholar
- Gould SJ: Dollo on Dollo’s Law: irreversibility and the status of evolutionary laws. J Hist Biol. 1970, 3 (2): 189-212. 10.1007/BF00137351.PubMedView ArticleGoogle Scholar
- Maddison WP, Midford PE, Otto SP: Estimating a binary character’s effect on speciation and extinction. Syst Biol. 2007, 56 (5): 701-710. 10.1080/10635150701607033.PubMedView ArticleGoogle Scholar
- Goldberg EE, Igic B: On phylogenetic tests of irreversible evolution. Evolution. 2008, 62 (11): 2727-2741. 10.1111/j.1558-5646.2008.00505.x.PubMedView ArticleGoogle Scholar
- Burnham KP: Multimodel inference: understanding AIC and BIC in model selection. Sociol Methods Res. 2004, 33 (2): 261-304. 10.1177/0049124104268644.View ArticleGoogle Scholar
- Crisp M, Cook L, Steane D: Radiation of the Australian flora: what can comparisons of moelcular pylogenies across multiple taxa tell us about the evolution of diversity in present-day communities?. Philos Trans R Soc Lond. 2004, 359: 1551-1571. 10.1098/rstb.2004.1528.View ArticleGoogle Scholar
- Schodde R: Origins, radiations and sifting in the Australasian biota: changing concepts from new data and old. Aust Sysematics Bot Soc Newsl. 1989, 60: 2-11.Google Scholar
- Lavin M, Herendeen PS, Wojciechowski MF: Evolutionary rates analysis of Leguminosae implicates a rapid diversification of lineages during the tertiary. Syst Biol. 2005, 54 (4): 575-594. 10.1080/10635150590947131.PubMedView ArticleGoogle Scholar
- Arroyo M: Breeding Systems and Pollination Biology in Leguminosae. Advances in Legume Systematics Part 2. Edited by: Polhill R, Raven P. 1981, Kew: Royal Botanic Gardens, 723-769.Google Scholar
- Joseph L, Toon A, Nyári ÁS, Longmore NW, Rowe KMC, Haryoko T, Trueman J, Gardner JL: A new synthesis of the molecular systematics and biogeography of honeyeaters (Passeriformes: Meliphagidae) highlights biogeographical complexity of a spectacular avian radiation. Zoologica Scripta. 2014, doi:10.1111/zsc.12049Google Scholar
- Schwarz MP, Fuller S, Tierney SM, Cooper SJB: Molecular phylogenetics of the exoneurine allodapine bees reveal an ancient and puzzling dispersal from Africa to Australia. Syst Biol. 2006, 55 (1): 31-45. 10.1080/10635150500431148.PubMedView ArticleGoogle Scholar
- Almeida EAB, Pie MR, Brady SG, Danforth BN: Biogeography and diversification of colletid bees (Hymenoptera: Colletidae): emerging patterns from the southern end of the world. J Biogeogr. 2012, 39 (3): 526-544. 10.1111/j.1365-2699.2011.02624.x.View ArticleGoogle Scholar
- Ödeen A, Håstad O: Pollinating birds differ in spectral sensitivity. J Comp Physiol A. 2010, 196: 91-96. 10.1007/s00359-009-0474-z.View ArticleGoogle Scholar
- Barker NP, Weston PH, Rutschmann F, Sauquet H: Molecular dating of the ‘Gondwanan’ plant family Proteaceae is only partially congruent with the timing of the break-up of Gondwana. J Biogeogr. 2007, 34 (12): 2012-2027. 10.1111/j.1365-2699.2007.01749.x.View ArticleGoogle Scholar
- Shrestha M, Dyer AG, Boyd-Gerny S, Wong BBM, Burd M: Shades of red: bird-pollinated flowers target the specific colour discrimination abilities of avian vision. New Phytol. 2013, 198 (1): 301-310. 10.1111/nph.12135.PubMedView ArticleGoogle Scholar
- Jesson LK: Ecological correlates of diversification in New Zealand angiosperm lineages. N Z J Bot. 2007, 45 (1): 35-51. 10.1080/00288250709509701.View ArticleGoogle Scholar
- Smith S, Miller R, Otto S, FitzJohn R, Rausher M: The Effects of Flower Color Transitions on Diversification Rates in Morning Glories (Ipomoea Subg. Quamoclit, Convolvulaceae). Darwin’s Heritage Today: Proceedings of the Darwin 2000 Beijing International Conference. Edited by: Long M, Gu H, Zhou Z. 2010, Beijing: Higher Education PressGoogle Scholar
- Futuyma DJ, Moreno G: The evolution of ecological specialization. Annu Rev Ecol Syst. 1988, 19: 207-233. 10.1146/annurev.es.19.110188.001231.View ArticleGoogle Scholar
- Hughes M, Moller M, Edwards TJ, Bellstedt DU, Villiers M: The impact of pollination syndrome and habitat on gene flow: a comparative study of two Streptocarpus (Gesneriaceae) species. Am J Bot. 2007, 94 (10): 1688-1695. 10.3732/ajb.94.10.1688.PubMedView ArticleGoogle Scholar
- Kramer AT, Fant JB, Ashley MV: Influences of landscape and pollinators on population genetic structure: examples from three penstemon (Plantaginaceae) species in the great basin. Am J Bot. 2011, 98 (1): 109-121. 10.3732/ajb.1000229.PubMedView ArticleGoogle Scholar
- Byrne M, Elliott CP, Yates C, Coates DJ: Extensive pollen dispersal in a bird-pollinated shrub, Calothamnus quadrifidus, in a fragmented landscape. Mol Ecol. 2007, 16 (6): 1303-1314. 10.1111/j.1365-294X.2006.03204.x.PubMedView ArticleGoogle Scholar
- Krauss SL, He T, Barrett LG, Lamont BB, Enright NJ, Miller BP, Hanley ME: Contrasting impacts of pollen and seed dispersal on spatial genetic structure in the bird-pollinated Banksia hookeriana. Heredity. 2009, 102 (3): 274-285. 10.1038/hdy.2008.118.PubMedView ArticleGoogle Scholar
- Ottewell KM, Donnellan SC, Lowe AJ, Paton DC: Predicting reproductive success of insect- versus bird-pollinated scattered trees in agricultural landscapes. Biol Conserv. 2009, 142 (4): 888-898. 10.1016/j.biocon.2008.12.019.View ArticleGoogle Scholar
- Cook LG, Crisp MD: Directional asymmetry of long-distance dispersal and colonization could mislead reconstructions of biogeography. J Biogeogr. 2005, 32 (5): 741-754. 10.1111/j.1365-2699.2005.01261.x.View ArticleGoogle Scholar
- Galis F, Arntzen JW, Lande R: Dollo’s Law and the irreversibility of digit loss in Bachia. Evolution. 2010, 64 (8): 2466-2476.PubMedGoogle Scholar
- Cronk QCB: Evolution in reverse gear: the molecular basis of loss and reversal. Cold Spring Harbor Symp Quant Biol. 2009, 74: 259-266. 10.1101/sqb.2009.74.034.PubMedView ArticleGoogle Scholar
- Orians GH, Milewski AV: Ecology of Australia: the effects of nutrient-poor soils and intense fires. Biol Rev. 2007, 82 (3): 393-423. 10.1111/j.1469-185X.2007.00017.x.PubMedView ArticleGoogle Scholar
- Ford HA, Paton DC, Forde N: Birds as pollinators of Australian plants. N Z J Bot. 1979, 17 (4): 509-519. 10.1080/0028825X.1979.10432566.View ArticleGoogle Scholar
- Pyke GH: The foraging behavior of Australian honeyeaters - a review and some comparisons with hummingbirds. Aust J Ecol. 1980, 5 (4): 343-369. 10.1111/j.1442-9993.1980.tb01258.x.View ArticleGoogle Scholar
- He TH, Lamont BB, Krauss SL, Enright NJ, Miller BP: Covariation between intraspecific genetic diversity and species diversity within a plant functional group. J Ecol. 2008, 96 (5): 956-961. 10.1111/j.1365-2745.2008.01402.x.View ArticleGoogle Scholar
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