Elsevier

Forest Ecology and Management

Volume 435, 1 March 2019, Pages 38-44
Forest Ecology and Management

Overlapping flowering periods among Shorea species and high growth performance of hybrid seedlings promote hybridization and introgression in a tropical rainforest of Singapore

https://doi.org/10.1016/j.foreco.2018.12.038Get rights and content

Highlights

  • Frequent hybridizations between dipterocarp species have occurred in fragmented forests.

  • Overlapping of flowering between F1 hybrids and related species have been observed.

  • Successive hybrid seedlings have higher growth performance than those of parents.

  • Successive hybridization potentially causes species loss through introgression.

  • It is important to consider the risk of hybridization for management of degraded forests.

Abstract

A considerable extent of interspecific hybridization among dominant canopy dipterocarp species was recently found in a tropical rain forest fragment in Singapore. However, information about the fertility of the hybrids and the growth of their successive hybrids remains limited. We studied the flowering phenology of four dipterocarp species in the genus Shorea (S. curtisii, S. leprosula, S. parvifolia, and S. macroptera) and two hybrids (S. curtisii × S. leprosula and S. leprosula × S. parvifolia) and studied the performances of seedlings reproduced from them. We observed that S. macroptera bloomed first, without overlap with congeneric species, followed by the other Shorea species and the two first filial (F1) hybrids. S. curtisii and S. leprosula, the species forming hybrids are most likely to succeed in this forest, completely overlapped with their hybrids. Fruits collected from the hybrids were viable, and these hybrid seedlings showed greater survival and a higher growth rate than those from pure species under greenhouse conditions. They included various cross types such as a backcross with each parent species. These results may imply that successive hybrids and introgression spontaneously occur among Shorea species. It may be important to consider the risk of hybridization for the management of tropical forests, particularly in degraded tropical rainforests where mechanisms of ecological isolation between closely related species might be altered.

Introduction

The extremely high species diversity of tropical rain forests in Southeast Asia is credited to the presence of large numbers of congeneric species that grow in sympatry (Ashton, 2014). A large proportion of the canopy trees in these forests belong to Dipterocarpaceae (dipterocarp trees, Ashton, 1982), and Shorea is one of the most speciose genera in this family (Ashton, 1982, Ashton, 2014, Symington, 2004). Reproductive isolation and habitat specialization of dipterocarp trees in the forest are thought to prevent interspecific crossing (Ashton, 1969, Ashton, 1982, Thomas, 2003, Kamiya et al., 2005, Ishiyama et al., 2008). However, in recent years, several hybrid trees of three closely related species of Shorea (S. curtisii, S. leprosula, and S. parvifolia) have been found in a small, isolated tropical rain forest in Bukit Timah Nature Reserve in Singapore (Kamiya et al., 2011, Kenzo et al., 2016). Surprisingly, approximately 20% of the hybrid trees that reached reproductive size (defined as diameter at breast height [DBH] > 30 cm) had two locally rare Shorea species (S. leprosula and S. parvifolia) as maternal parent species, but the frequency of hybridization of a much more abundant species, S. curtisii, was less than 2% (Kamiya et al., 2011). Moreover, the rate of F1 seedlings and saplings of these species in Bukit Timah reached 40% (Kenzo et al., 2016).

Forests in Singapore have been subjected to anthropogenic fragmentation for more than 150 years, and the Bukit Timah forest (164 ha) is considered one of the oldest fragmented tropical rain forests in the area (Corlett, 1988). Although there are no clear factors in explaining this very high rate of hybridization in the forest, it is possible that forest fragmentation and degradation, which are also progressing rapidly throughout Southeast Asia (Hansen et al., 2013), may promote hybridization due to a decrease in mother tree density, pollinator overlap, and environmental changes (e.g. increased edge effects by forest fragmentation) that encourage the performance of hybrid seedlings (Rieseberg et al., 1989, Lamont et al., 2003, Field et al., 2008, Wong and Low, 2011, Kenzo et al., 2016).

Temporal separation of flowering timeings is a key mechanism that isolates species of Dipterocarpaceae from each other (Ashton, 1982, Ashton, 2014, Ashton et al., 1988, Ghazoul, 2016), but the separation might be incomplete as several hybrid Shorea species have been found (Kamiya et al., 2011). Most dipterocarp species bloom simultaneously during the general flowering period (∼6 months), which is observed at 2- to 10-year intervals in the region (Ashton, 1982, Sakai et al., 2006), but the flowering peak for each dipterocarp species occurs sequentially (Ashton et al., 1988, Ghazoul, 2016). In the genus Shorea, the possibility of interspecific crossing exists due to the behavior of common pollinators including thrips, stingless bees, honeybees, and beetles (Appanah and Chan, 1981, Momose et al., 1998, Sakai et al., 1999, Ashton, 2014). If the hybrid trees are fertile and their flowering periods overlap with those of the parental species, successive hybridization and introgression would be promoted in Shorea species. However, even if hybrid trees are fertile, it is possible that their descendants may be maladaptive. Therefore, it is also important to assess the initial performances of parent species and their hybrid offspring at the seedling stage in understanding and predicting the progress of future hybridization (Arnold, 2006). Although naturally occurring F1 hybrid seedlings in Shorea species have similar growth performances to those of their parent species in the forest understory (Kenzo et al., 2016), successive hybrids, such as those of backcrosses and F2 generations, may have high growth performances that are advantageous to regeneration.

For example, Schweitzer et al. (2002) found that F1 hybrids demonstrated relatively low fitness, but that naturally occurring backcrosses (BC) and the experimentally produced second generation of backcross (BC2) had relatively high fitness. If seedlings which are derived from F1 hybrid mother trees are viable and show growth comparable to that of parent trees, high rates of hybridization among dipterocarp species and the existence of adult hybrid individuals at high frequency in the forest might eventually lead to loss of species through the consolidation of distinct gene pools by introgression (Levin et al., 1996, Orians et al., 1999, Arnold, 2006, Kettle et al., 2012). However, few studies have examined the ecological traits of hybrids and their offspring (Kamiya et al., 2011, Kenzo et al., 2016).

In this study, we addressed two questions: Is there a difference in the flowering period between adult F1 hybrids and their parent species?; and do seedlings derived from the mother trees of parent species and F1 hybrids have different growth performances and viabilities? To answer these questions, we observed the flowering phenology of four species in the section Mutica of the genus Shorea and two pairs of their hybrids in the Bukit Timah forest. In addition, we collected seeds from hybrid mother trees and parent species and evaluated the initial growth performances at the seedling stage under nursery conditions.

Section snippets

Study site

Our study was conducted in a coastal hill dipterocarp forest in the Bukit Timah Nature Reserve (1°21N, 103°46E) in Singapore. The area has a humid tropical climate with no clear seasonal patterns in rainfall (Fig. 1, annual mean: 2,473 mm) nor temperature (annual mean: 27 °C) (Lum et al., 2004). The forest is a fragment that has persisted in a landscape impacted by anthropogenic activities for more than 150 years (Corlett, 1988). It presently has an area of 164 ha, of which 48–71 ha is intact

General flowering in Bukit Timah in 2009

We observed a total of 208 trees during the general flowering event in 2009 (Table 1). The percentage of flowering trees was less than 30% in S. curtisii, S. leprosula, and S. macroptera. Only 2 of the 18 S. leprosula × S. curtisii hybrids and 1 of the 2 S. leprosula × S. parvifolia hybrids flowered, whereas the only S. curtisii × S. parvifolia hybrid did not flower (Table 1). Nine out of ten (90%) S. parvifolia trees flowered. The peak flowering of Shorea occurred from March to May (Fig. 2).

General flowering in Singapore

The severe drought which occurred in January 2009 might have induced the flowering of dipterocarp trees in Singapore as a trigger. Recent studies also reported that severe drought prior to flowering had acted as a trigger for general flowering in the Malay Peninsula and Borneo (Sakai et al., 2006, Ashton, 2014, Ghazoul, 2016). Corlett (1990) also reported from Bukit Timah that they had observed a severe drought in February 1987 (rainfall; 24.5 mm between 30 January and 3 March) and this may

Conclusions

We found that the flowering periods of the F1 hybrids (S. curtisii × S. leprosula and S. leprosula × S. parvifolia) overlapped with those of their parent species (S. curtisii, S. leprosula, and S. parvifolia). This may imply that the F1 may be able to hybridize further with their parental species, resulting in their increased introgression. This is concordant with the fact that the seeds collected from the S. curtisii × S. leprosula hybrid were viable and their seedlings had high growth

Acknowledgements

We thank the National Parks Board, Center for Tropical Forest Science – Arnold Arboretum Asia Program, Nature Heritage Group in the Japanese Association Singapore, and the National Institute of Education, Nanyang Technological University, Singapore, for their kind support of this study. This study was conducted under permission from National Parks Board, Singapore (NP/RP 857 and 972-1 to 972-7). This work was partly supported by JSPS KAKENHI Grants (No. 21780155, No. 21688011, No. 24405032, No.

References (57)

  • Ashton, P.S., 1982. Dipterocarpaceae. Flora Malesiana 9,...
  • P.S. Ashton et al.

    Staggered flowering in the Dipterocarpaceae: new insights into floral induction and the evolution of mast fruiting in the aseasonal tropics

    Am. Nat.

    (1988)
  • P.S. Ashton

    On the Forests of Tropical Asia: Lest the Memory Fade

    (2014)
  • F.Q. Brearley et al.

    Reproductive phenology over a 10-year period in a lowland evergreen rain forest of central Borneo

    J. Ecol.

    (2007)
  • P.F. Burgess

    Studies on the regeneration of the hill forests of the Malay Peninsula

    Malay. For.

    (1972)
  • C.H. Cannon et al.

    Variable mating behaviors and the maintenance of tropical biodiversity

    Front. Genet.

    (2015)
  • H.T. Chan et al.

    Reproductive biology of some Malaysian dipterocarps I: flowering biology

    Malay. For.

    (1980)
  • Y.Y. Chen et al.

    Species-specific flowering cues among general flowering Shorea species at the Pasoh Research Forest, Malaysia

    J. Ecol.

    (2017)
  • R.T. Corlett

    Bukit Timah: the history and significance of a small rain-forest reserve

    Environ. Conserv.

    (1988)
  • R.T. Corlett

    Flora and reproductive phenology of the rain forest at Bukit Timah, Singapore

    J. Trop. Ecol.

    (1990)
  • D.L. Field et al.

    Relative frequency of sympatric species influences rates of interspecific hybridization, seed production and seedling performance in the uncommon Eucalyptus aggregata

    J. Ecol.

    (2008)
  • J. Ghazoul

    Dipterocarp Biology, Ecology, and Conservation

    (2016)
  • M.C. Hansen et al.

    High-resolution global maps of 21st-century forest cover change

    Science

    (2013)
  • K.O. Irino et al.

    Effects of controlled-release fertilizer on growth and ectomycorrhizal colonization of pot-grown seedlings of the dipterocarp Dryobalanops lanceolata in a tropical nursery

    Soil Sci. Plant Nutr.

    (2004)
  • H. Ishiyama et al.

    Demographic history and interspecific hybridization of four Shorea species from Peninsular Malaysia inferred from nucleotide polymorphism in nuclear gene regions

    Can. J. For. Res.

    (2008)
  • K. Kamiya et al.

    Phylogeny of PgiC gene in Shorea and its closely related genera (Dipterocarpaceae), the dominant trees in Southeast Asian tropical rain forests

    Am. J. Bot.

    (2005)
  • K. Kamiya et al.

    Morphological and molecular evidence of natural hybridization in Shorea (Dipterocarpaceae)

    Tree Genet. Genomes

    (2011)
  • K. Kamiya et al.

    Demographic history of Shorea curtisii (Dipterocarpaceae) inferred from chloroplast DNA sequence variations

    Biotropica

    (2012)
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