不稔性分類群の起源
Origin of the sterile taxa in Lycoris

Species Evolution by Hybridization in the genus Lycoris, Amaryllidaceae

Siro Kurita, Emeritus Professor
Department of Biology, Faculty of
Science, Chiba University, Japan


INTRODUCTION

 The royal road to species evolution is gene mutation and isolation, but thehybridization also bears very important role of the speciation.
 The possibility of new species formation by hybridization was already noticed in the mid-eighteenth century as reported by Linnaeus and Rudberg in Linaria, Scrophulariaceae (Linnaeus, 1760). 
 Most research workers at that time, however, made little account of the evolutionary role of hybridization until the early twentieth century because of the sterility of the interspecific hybrids. They considered that the hybrid is the blind alley of evolution.
 The situation dramatically changed by verification of Winge’s hypothesis (Winge, 1917). He proposed the fruitful hypothesis of chromosome number doubling in interspecific hybrids. Winge’s hypothesis was soon confirmed experimentally by artificial interspecific hybridizations in Nicotiana, Raphanus-Brassica, and Galeopsis (Clausen and Goodspeed, 1925; Karpechenko, 1927; Muntzing, 1932).
 Recent researchers have recognized the significance of hybrid speciation for evolution and the essential part of the mechanism of hybrid speciation is the stabilization of breeding behavior of the hybrids. At present various methods of stabilization in hybrid reproduction are known. The methods are:

(1)   vegetative propagation; (2) agamospermy; (3) amphiploidy; (4) permanent odd polyploidy; (5) permanent translocation heterozygosity; (6) recombinational speciation; and (7) the segregation of a new genotype isolated by external barriers (cf. Grant, 1981).

At present, two methods, (1) and (7) are recognized among the hybrids of the genus Lycoris.

 Lycoris is an endemic genus to Sino-Japanese flora. It consists of about 13 fertile taxa (2n=12, 14, 16, 22: NF=22) and 14 or more sterile taxa (2n=13, 15, 17, 18, 19, 23, 27, 29, 30, 31: NF=22, 23, 32, 33), excepting for several artificial hybrids produced by horticulturists. These taxa are distributed in warm temperate to subtropical zone of East Asia from southwestern China to Japan and southern Korea、 with a few extending to northern Indochina and Nepal.


 OBSERVATION AND DISCUSSION

 In the karyological point of view, the fertile taxa can be divided into two groups.

 The first group has the genomes consisting of large metacentric chromosomes and telocentric chromosomes. The [M+T] is the brief account of this genome.
 In this group L. traubii (2n=12=10M+2T, 14=8M+6T), L. aurea (2n=14=8M+6T, 16=6M+10T), L. longituba (2n=16=6M+10T), L. anhuiensis (2n=16=6M+10T), L. chinensis (2n=16=6M+10T) and the hybrid swarm (2n=16=6M+10T) of L. longituba X L. chinensis are included.

The second group has the genomes consisting of 11 acrocentric chromosomes. L. sanguinea, L. sprengeri, L. rosea, L. haywardii, and L. radiata var. pumila are included in this group (2n=22=22A). The [A] is an abridgement of this acrocentric genome.

On the other hand, excepting a few autopolyploids such as L. radiata, almost all of the sterile taxa have both [M+T] and [A] type genomes, which supposed to be originated in hybridization between the species having [M+T] and that having [A].

Species of the genus Lycoris are easily hybridized; diverse morphological features occur frequently among them in nature and in cultivation.

 In Japan, species are distributed. Among them, only two species, L. traubii and L. sanguinea, are fertile species which can propagate by seeds. The rest of five are sterile species which propagate exclusively by division of bulbs.
 In Korea, 6 species are known among which L. koreana and L. chinensis var. sinuolata are fertile.
 In China, the center of distribution of this genus, 16 or more species are described. Among them 8 species are fertile. Therefore, approximately half of the described species of the genus are sterile.
 All of these sterile species are supposed to be originated in hybridization.

Japanese Flora:

 (1) L. albiflora : 
  This highly sterile species is distributed in southwestern part of Kyushu. 
  As to the origin of this sterile species, Inariyama (1932, 1933, 1937) considered that it might be a hybrid between L. sanguine (2n=22=22A) and L. traubii (2n=12=10M+2T) according to the cytological point of view. While, Makino (1943) supposed it a hybrid between L. radiata (2n=33=33A) and L. traubii based on its gross morphology.
 Inariyama (1944) rectified his previous conclusion and advocated that the parents of this species are L. traubii and L. radiata var. pumila (2n=22=22A) which is distributed in China.
  The karyotype of L. albiflora, 2n=17=5M+1T+11A, is not consistent with Inariyama’s supposition, but this supposition is doubted at the phytogeographical and phenological point of view.
  At present, L. albiflora is endemic to Japanese flora and L. radiata var. pumila is not found in Japan, but China.
  Moreover, if L. radiata var. pumila was distributed in Japan in the past, it is very difficult to cross with L. traubii.  Because L. radiata var. pumila blooms towards the end of August while L. traubii blooms at the beginning of October.
  Recent studies support the intuitive Makino’s hypothesis.
 The supposed parents, L. radita and L. traubii distribute sympatrically in Kyushu, and the blooming period of both species overlaps.
 Though the meiosis of triploid L. radiata is irregular, it produces viable pollens on rare occasions (Koyama, 1959). Such pollen has the normal genome consisting of 11 A type chromosomes.
 Therefore, the karyotype, 2n=17= 5M+1T+11A , of L. albiflora supposed to be the result of the fertilization between a gamete (5M+1T) of L. traubii and a gamete (11A ) of L. radiata (Kurita, 1987).

 (2) L. rubroaurantiaca
    This sterile species is restrictedly found in southwestern Kyushu, especially Satsuma and Osumi peninsular, Kagoshima Prefecture. The origin of this was studied circumstantially by Ueno et al. (1994).
  They revealed that the parents of L. rubroaurantiaca (2n=17=5M+1T+11A) are L. traubii (2n=12=10M+2T) and a forma of L. sanguinea which blooms in autumn (2n=22=22A).

Korean Flora
 

 1)   L. flavescens
    This taxon was descried as a new species by Kim, M.Y. and Lee, S.T. in 1991 (K.J.P.T., 21(2)), and they suggested that this species was originated in hybridization between L. koreana and L. chinensis.
   Soon, I rigidly supported this hypothesis in the symposium at the XV International Botanical Congress in 1993 (cf. Sino-Japanese Flora; Its Characteristics and Diversification. Univ. Mus., Univ. Tokyo, Bull. 37, 1998).
  It is reasonable to suppose that a genome, 11A, in L. flavescens was originated from L. koreana and another genome, 3M+4T+1sm, from L. chinensis.
   The karyotype of Korean L. chinensis is very unique. The submetacentric chromosome (sm) is not included in that of typical L. chinensis from China. The sm chromosome should be produced by pericentric inversion of T type chromosome in the genome of typical L. chinensis.
   At the gross morphological point of view, it is very difficult to distinguish Korean L. chinensis from the typical Chinese plant. The karyotype, however, quite distinct. So, Tae and Ko (1993) recognized this Korean plant as L. chinensis var. sinuolata.

2) L. chejuensis :
    In the symposium, Floristics and Phytogeography, at the XV International Botanical Congress in 1993 in Yokohama, Hsu and Kurita reported this taxon to be a new species, which originated in hybridization between L. koreana and L. chinensis. In the same year Tae and Ko (1993) described authentically this taxon as a new species, L. chejuensis.
   Tae and Ko (1993) emphasized the distinct cytological character and reported 2n=30=3V+27R (V means v-shaped and R means rod-shaped chromosomes). However, they did not discuss the origin of this new species.
   Gross morphology of this species is intermediate of L. koreana and L. chinensis. The karyotype strongly suggests that an unreduced gamete (22A) of L. koreana united with a reduced gamete (3M+4T+1sm) of Korean L. chinensis.


Chinese Flora:

  China, especially the drainage basin area of the Yangtze-Kiang, is the center of speciation of the genus, in where six fertile stem species are known. They are L. radiata var. pumila, L. sprengeri, L. aurea, L. longituba, L. chinensis, and L. anhuiensis.

1)  L. radiata var. pumila X L. chinensis  
    I collected five sterile taxa at Mt.Mogan, Zejiang Province. These sterile taxa are found in the area where two fertile stem species, L. chinensis (2n=16=6M+10T) and L. radiata var. pumila (2n=22=22A) are distributed sympatrically.
  The floral morphology of these sterile taxa is very variable, but the karyotype is uniform. All examined plants in the above pictures have the same karyotype, 2n=19=3M+5T+11A. And each sterile plant is found in the population of L. chinensis or L. radiata var. pumila as shown in these figs.
  Therefore, these sterile taxa are supposed to be the hybrid between L. chinensis (6M+10T) and L. radiata var. pumila (22A).

In Mt. Mogan, two more interesting sterile taxa were collected. 
 The karyotype of one taxon is very similar to that of L. flavescens, 3M+4T+1sm+11A, but the floral morphology is dissimilar.
  At the gross morphological point of view, this plant is also supposed to be a hybrid between L. chinensis and L. radiata var. pumila. And the existence of submetacentric chromosome (sm) in this hybrid plant suggests the probability of distribution of L. chinensis var. sinuolata (2n=16=6M+8T+2sm) in this area.

 Another interesting taxon is triploid. The karyotype is 2n=30=3M+5T+22A. The same karyotype was reported in L. houdyshelii (Bose, 1957; Kurita, 1987).
  The floral morphology and foliage character of this taxon, however, do not accord with those of L. houdyshelii.

2)  L. chinensis X L. sprengeri  2n=19=3M+5T+11A
    I collected three sterile taxa in Shiangjuandon area near Yixing city, Jiangsu Province. In this area, three fertile stem species, L. chinensis, L. sprengeri, and L. radiata var. pumila are found.
  The plant of type A was collected in a population of L. sprengeri. The morphology and cytology of type A accords with those of L. cv. off-white (Kurita et al., 1992). The type B and type C were collected in a large population of L. chinensis. As shown in above figures, these plants possess the same chromosome number, 2n=19, and their karyotype, 3M+5T+11A, is identical.
  These data suggest that the plants of type A, B and C are the hybrids between L. sprengeri and L. chinensis.

3)  Other sterile species originated in Chinese flora.

a) L. straminea 2n=19=3M+5T+11A
  This sterile species is found in Jiangsu and Zhejiang Province. The karyotype analysis of this species suggests that it may also be of hybrid origin, and the type specimens were probably from segregates of the F1 progeny of L. radiata and the species with 2n=16=6M+10T. The floral character is intermediate of L. chinensis or L. anhuiensis and L. radiata.

b) L. incarnata  2n=30=3M+5T+1M’+20A+1m
  The origin of this sterile species is very problematical. This karyotype may originate from a cross between a gamete with 3M+5T and another gamete with 1M’+20A+1m.
  Recently this species was found in Anduk Valley, Cheju Is. (Roh, et al., 2002). Its karyotype is the same as Chinese materials.

c) L. houdyshelii  2n=30=3M+5T+22A
  No record of wild plants of this species. The type material was imported into USA from a Chinese nurseryman in Shanghai, in 1948. The character of flower and leaf suggests that a parent of this sterile species is L. longituba, the donor of a gamete with 3M+5T. Another parent, the donor of unreduced 22A genome, is quite unknown. The plant with the same karyotype was found in Mt. Mogan, but the floral morphology is different.

d) L. cardwellii  2n=27=6M+10T+11A
  The bulbs of this sterile species are also found in the shipment out of Shanghai, before 1949. The gross morphology of this hybrid similar to that of L. houdyshelii, but the karyotype is distinct. This plant may be originated in crossing between an unreduced gamete with 6M+10T and a reduced gamete with 11A, or between a reduced gamete with 3M+5T and an unreduced with 3M+5T+11A of a hybrid species such as L. straminea.

e) L. squamigera   2n=27=6M+10T+11A
  In China, this sterile plant distributes in southeastern region, Jangsu, Shandong and Zhejiang Province. In Korea and Japan, it also common, but it occurs only in gardens or human habitation as an escape. Although the karyotype of this species is identical with that of L. cardwellii, the gloss morphology is very different each other.
  The origin of this plant was studied by Inariyama (1953) and Takemura (1961). They concluded that it is a hybrid between L. sprengeri (n=11A) and L. straminea sensu Inariyama (= L. longituba, 2n=6M+10T). This conclusion is not contradicting the cytological and morphological features. As well as the origin of L. cardwellii, however, there is another interpretation that the karyotype of L. squamigera may originate from the cross between 3M+5T and 3M+5T+11A, an unreduced gamete of unknown sterile taxon.

f) L. aurea sensu stricto  2n=15=7M+8T
  The karyotype of L. aurea sensu stricto is intermediate of “8M+6T” and “6M+10T”. At the cytological point of view, this sterile plant seems to be a hybrid between two fertile taxa, 2n=14 and 2n=16, or a race originated from the Robertsonian change in one M type chromosome. 
  However, floral and vegetative characters of this sterile plant are very distinctive.
 Additional phytogeographical, cytological and molecular survey on L. aurea sensu lato should be clarifying this controversial species problem.

4) Semisterile taxa
   In Chinese flora 3 or more semisterile taxa are found. Their karyotype  is 2n=22=22A or 2n=16=6M+10T. These taxa produce a few seeds under cultivation, but the fertility of these seeds is low so far as I know.

a) L. rosea   2n=22=22A
  This species is distributed in sparse second growth forest of low hills in Jiangsu Province. It seems to be a natural hybrid between L. sprengeri and L. radiata var. pumila. Lin et al. (unpub.) made a crossing between the two taxa and obtained many F1 plants, of which three accord well with L. rosea in gross morphology.

b) L. haywardii  2n=22=22A
  This species is only known in cultivation. Five plants among the F1 plants obtained by Lin et al. (unpub.) resemble this species very much in gross morphology and karyotype.

c) L. longituba x L. chinensis ?  2n=16=6M+10T
  This plant was found in a population of L. longituba at Tangshan, near Nanjing, Jangsu Province. The floral morphology of this plant is intermediate of L. longituba and L. chinensis which is rather common around Nanjing. The karyotype, 2n=16=6M+10T, of this plant supposed to be a product of the crossing between L. longituba (6M+10T) and L. chinensis (6M+10T). It is not conflict with the gross morphology of this plant.
  Under cultivation, this intermediate plant sets a few seeds which can germinate.
  In Nanjing Chunshan Botanic Garden, many bulbs of L. longituba and L. chinensis are in cultivation as ornamentals, and various intermediate plants are growing around them. Some are very much similar to the Tangshan intermediate.

CONCLUSION

Speciation Patterns in Lycoris

1.       Successive speciation:

The species evolution of sexually reproducing fertile taxa such as L. sprengeri (2n=22=22A) and L. chinensis (2n=16=6M+10T) should be successive. The formation of two or more reproductively isolated species from a common ancestral breeding population by accumulation of mutations and geographical isolation is a time-consuming process. The existence of variable fertile species in Lycoris at present may be the result of successive speciation.

2.       Extemporaneous speciation:

 In this genus, new species are frequently formed extemporaneously by fusion of heterogeneous gametes. These new species propagate exclusively by fission of their bulbs. Three types are recognized.

a)       Autotriploidy:
 At present, autotriploid taxa are reported in three species; L. radiata, L. sanguinea and L. sprengeri. These triploid plants are supposed to be autotriploid, which is produced by fusion of a gamete with 11A and a nonreduced gamete with 22A. This hypothesis was supported by karyotype analysis and meiotic behavior forming trivalent chromosomes.
 On the other hand, no autotriploid plants are known in the group with M+T type genome. What can be the reason? It is an enigma.

b)      Hybridization -1:
   Speciation by crossing between two fertile species:
      Hybrids between [A]and [M+T] type genomes.
       3M+5T + 11A -----L. chinensis X L. rad. var. pumila complex
                      L. chinensis X L. sprengeri complex
                      L. flavescens (inc. 1sm.)
                      L. straminea, etc.
      5M+1T + 11A ---  L. albiflora, L. rubroaurantiaca, L. elsiae

       4M+3T + 11A ---- L. cv. satumabijin
       3M+5T + 22A ----  L. houdyshelii, L. incarnata, L. chejuensis
      6M+10T + 11A ----L. squamigera, L. cardwellii


      Hybrids among [A] or [M+T] type genomes:
       3M+5T + 3M+5T  ------L. longituba X L. chinensis complex
       3M+5T + 4M+3T  ----- L. aurea var. aurea
       11A   +  11A   ------ L. rosea, L. haywardii, etc.

c)        Hybridization -2:
    Speciation by crossing among hybrids or between hybrid and fertile taxon: 
    It is very difficult to detect this type of hybrids by karyotype analysis and morphological study in wild population. Horticulturists, however, successes to obtain various cultivars of this type of hybrids by cross pollination. For example, Lin, J.Z. at Hangzhou Botanic Garden crossed L. radiata var. pumila () with L. straminea (), and she got some F1 plants. One bulb among them has the karyotype of 2n=23=1T+22A. This F1 plant may be formed by fusion of a gamete with 1T+11A from L. straminea and 11A from L. radiata var. pumila.

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