Overlapping flowering periods among Shorea species and high growth performance of hybrid seedlings promote hybridization and introgression in a tropical rainforest of Singapore
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°21′N, 103°46′E) 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.
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