Oecologia (2006) 149:428–443 DOI 10.1007/s00442-006-0461-9
PL AN T AN IM AL IN TE R ACT IO N S
Dietary specialization in European species groups of seed beetles (Coleoptera: Bruchidae: Bruchinae) Bernard Delobel · Alex Delobel
Received: 14 December 2005 / Accepted: 26 April 2006 / Published online: 23 June 2006 © Springer-Verlag 2006
Abstract Because of their particular biology, seed beetles exhibit a strong relationship with their larval host plants. In Europe, however, Weld data have long been scarce and unreliable. The results of Legume seed collections of nearly 1,000 samples belonging to 292 species from various locations in Europe are summarized. The status of current Bruchidius species groups is amended on morphological and phylogenetic bases. Recent advances in the knowledge of phylogenetic structures of both Fabaceae and Bruchinae provide a new picture of Bruchinae–Fabaceae interactions. It reveals a certain level of host conservatism. The hypothesis of radiative adaptation seems the most compatible with observed data. Keywords Bruchidius – Bruchus · Diet breadth · Species group · Speciation
Communicated by Volkmar Wolters According to currently accepted phylogenies, seed beetles constitute a sister group to Sagrinae within the family Chrysomelidae (see discussion in Lingafelter and Pakaluk 1997). For convenience, we have, however, retained the name Bruchidae. B. Delobel Laboratoire BF21, Bâtiment Louis Pasteur, INRA/INSA, 69621 Villeurbanne Cedex, France A. Delobel (&) Muséum national d’Histoire Naturelle, Entomologie, 45 rue BuVon, 75005 Paris, France e-mail:
[email protected]
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Introduction Seed beetles have been used for a number of years as a model for the study of host plant use because of a strong and unique relationship between individual insects and their host plants, and also because ecological and biological data are easily obtainable by rearing larvae within the host seed. Attempts to identify and evaluate factors involved in cladogenesis and species diversiWcation in several groups of seed beetles have recently been undertaken (Kergoat et al. 2004, 2005a, b; Morse and Farrell 2005). Updated biological data on Bruchinae (identiWcation of new host plants and clariWcation of the host status of plants mentioned in older records) were given by Delobel and Delobel (2003, 2005). One major goal of these studies was to assess the role of host plants in speciation mechanisms, and also the impact of other factors such as ecology, biogeography, or climatic events. Ehrlich and Raven’s (1964) paper was a landmark in the study of the evolution of relationships between phytophagous insects and their host plants. According to their model of codiversiWcation and cospeciation, reacting chemical defences of plants and insects are supposed to lead to an ever-increased specialization of phytophagous insects on increasingly specialized hosts. Their ideas have, however, recently been the object of much questioning. In a sample of 50 African species of Bruchidius exhibiting a high level of taxonomic conservatism (Kergoat et al. 2005a), the hypothesis of cospeciation was not supported by available biological data. At the subfamily level, the two phylogenies were not congruent, and Caesalpinioideae appeared as secondarily acquired hosts, whereas primary hosts were Mimosoideae that evolved from Caesalpinioid ancestors.
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Similarly, closely-related species were found to predate on Indigofereae and Phaseoleae, two unrelated tribes. The impact of secondary compounds contained in seeds and pod walls on bruchid development has long been recognized (see Southgate 1979). In the case of a selected group of seed beetles predating upon Mimosoideae, a close relationship was found between bruchid phylogeny and the nature of noxious secondary compounds in the seeds on which they feed (Kergoat et al. 2005a). Similarly, whereas Wdelity to single genera or at most subtribes was demonstrated in a group of Asian Callosobruchus species (Tuda et al. 2005), important variations in the level of polyphagy were observed, with a few polyvoltine cosmopolitan species feeding all year round on stored pulses belonging to unrelated genera. In much the same way, Morse and Farrell (2005) showed, in the New World genus Stator, a wide variety of diet breadths, host aYliations, and in the stage at which seeds were attacked. Specialized as they may be, seed beetles may retain a large capability to use alternative hosts, and may well be able to undergo a radiation on them. As stressed by Johnson (1981a), identiWcation of insect–plant relationships in a large proportion of species in a given genus is a prerequisite to further progress in this Weld. This is possible only if reliable data are obtained from larval rearings, and accurate identiWcations of both botanical and entomological specimens are performed. IdentiWcation of Old World bruchids has long been hindered by taxonomic misinterpretations and misidentiWcations. Major progress in European bruchid taxonomy was due to Wendt (1978, 1992), Borowiec (1988), Borowiec and Anton (1993) and Anton (1994, 1998, 1999). As a result, partial phylogenetic reconstructions were recently proposed for Bruchus and Bruchidius, which are the two main genera of Bruchinae in the area (Kergoat et al. 2004). A good agreement was found between morphological characterization of species groups as deWned by Borowiec (1988) and phylogenetic hypotheses based on molecular data (Table 1). The great majority of European Bruchinae are Legume feeders and, more speciWcally, Faboideae feeders. Only a few species predate on non-Legume seeds: B. cinerascens (Gyll.) on Apiaceae, B. biguttatus (Olivier) and probably B. cisti (F.) on Cistaceae. Delimitations of sections and genera of Faboideae in Fig. 1 and Tables 2, 3, 4, 5 and 6 are the result of recent phylogenetic studies, reviewed by Wojcechowski (2003) and Wojcechowski et al. (2004). Major modiWcations introduced in the botanic groups concerned may be summarized as follows: Cubas et al. (2002) and Pardo et al. (2004) have modiWed the perception of generic delimi-
429 Table 1 West European Bruchinae species groups as established by Borowiec (1988) and Anton (1998) Species groups
Species included
Bruchidius serraticornis
jocosus, meleagrinus, rubiginosus bituberculatus, borowieci, lividimanus, mulsanti, pusillus, seminarius, taorminensis, villosus biguttatus, pauper cisti, lutescens, olivaceus, poupillieri, unicolor bernardi, caninus, marginalis, varipes annulicornis, dispar, fulvicornis, imbricornis, martinezi, picipes, poecilus, varius bimaculatus, nanus calabrensis, murinus cinerascens tibialis, longulus foveolatus, pygmaeus, sericatus gilvus aVinis, viciae atomarius, dentipes, ruWmanus loti griseomaculatus, libanensis, luteicornis, occidentalis, ruWpes brachialis, ibericus, laticollis, signaticornis, ulicis, venustus emarginatus, lentis, pisorum tristiculus, tristis
Bruchidius seminarius
Bruchidius pauper Bruchidius unicolor Bruchidius astragali Bruchidius varius
Bruchidius bimaculatus Bruchidius murinus Bruchidius cinerascens Bruchidius tibialis Bruchidius foveolatus Paleoacanthoscelides Bruchus aVinis Bruchus atomarius Bruchus loti Bruchus ruWpes
Bruchus brachialis
Bruchus pisorum Bruchus tristis
Species not present in the geographic area were excluded
tations in Genistoids, but taxon names have not yet been updated. All published results agree on the fact that Adenocarpeae constitute a distinct subgroup, sister of all other Cytiseae. Loteae in the present sense results from the jointure of Loteae sensu stricto and Coronilleae (Polhill 1981; Allan et al. 2003; Nanni et al. 2004). The last group (Vicioids plus Medicagoids) is composed of former Trifolieae plus Vicieae. Multiple phylogenetic studies (Wojciechowski et al. 2000) show that Trifolium is more closely related to Vicieae than to Medicago and allies, so that the group is now divided in three parts: Medicagoids, the genus Trifolium, and Vicieae. Medicagoids are still the object of taxonomic debate. Even after moving some Trigonella species to Medicago (Small 1987), a continuum exists from morphological, chemical and molecular (Bena et al. 1998) points of view. The inside structure of the clade Trifolium shows the Chromosemium section sister of all the other
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Fig. 1 Strongly pruned phylogenetic tree showing main Papilionid clades, after Wojciechowski et al. (2004). Clades containing plants native to Europe. All these clades are exploited by European Bruchinae. Within Robinioids, genus Sesbania, sister clade of Loteae, is exploited by Bruchidius chloroticus (Dalman) in Africa and Asia, by B. schoutedeni (Pic) in Central and Western Africa. In the Robinia clade, only the polyphagous Stator pruininus (Horn) predates on seeds of Coursetia, Olneya and Robinia spp. in America (Center and Johnson 1976; Johnson and Kingsolver 1976; Morse and Farrell 2005). A few records of Old World Bruchidius sp. feeding on Robinia pseudoacacia seriously need conWrmation (e.g., Morimoto 1990). Robinia (= Halimodendron) halodendri, the seeds of which are predated upon by Bruchidius halodendri in Central Europe (Lukjanovitch and Ter-Minassian 1957) belongs to the Astragalean tribe
Trifolium, and then T. subterraneum sister species of all remaining Trifolium sections (Steele and Wojciechowski 2003). The phylogeny of the latter is not completely resolved and remains controversial (Watson et al. 2000). T. repens, an allotetraploid hybrid (Badr et al. 2002b) and formerly a member of the Trifoliastrum section, is now closer to North American Trifolium (Steele and Wojciechowski 2003). The Vicieae tribe is composed of four genera dispatched in two groups: Vicia plus Lens, and Lathyrus plus Pisum. Lathyrus infrageneric structure as deWned by Kupicha (1983) was amended following molecular studies (Asmussen and Liston 1998; Badr et al. 2002a), which showed close relationships between Lathyrus section and Orobastrum, Pratensis and Aphaca sections, and conWrmed the homogeneity of Orobus section. The latter shares ancestors with section Clymenium + Nissolia. Lathyrostylis and Linearicarpus sections are two close sister clades (Kenicer et al. 2005) and were therefore consid-
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ered together. Vicia is divided in two subgenera, Vicia and Vicilla (Kupicha 1976). Johnson (1981a) was the Wrst to attempt a classiWcation of Legumes based on bruchid host speciWcity. The state of botanical and entomological knowledge was such at the time that the task turned out to be quite diYcult. Very signiWcant advances in both Welds make it possible to renew Johnson’s endeavor. We shall identify host plant use based on results (including negative data) of Weld sampling of potential host plants in Portugal, Spain, France, Italy, and Greece, part of which were published earlier (Delobel and Delobel 2003, 2005). Reliable data from recent literature (Jermy and Szentesi 2003) will also be included. We shall attempt to identify and explain the limits of taxonomic conservatism in European Bruchinae, using clades proposed by the more recent phylogenetic hypotheses on one hand, and on Legume clades presently accepted by most botanists on the other. An examination of the various types of interactions between bruchids and their host plants as brought to light by our data will be performed.
Materials and methods Nearly ripe or ripe pods/seeds of Legumes were collected in the wild all over France (2001 and onwards), southern Italy (Basilicata and Calabria) in 2003, southern Greece (Korynthos, Lakonia, Voiotia, Fokkida, Arkhadia) in 2004, Spain (Almeria, Malaga, Granada, Caceres) and Portugal (Algarve and Alentejo) in 2005. A total of 950 samples corresponding to 292 plant species were collected and identiWed. Bibliography and Xoras used for identiWcation of French, Italian and Greek samples were reported in Delobel and Delobel (2003, 2005). For the 2005 collections in Spain and Portugal, plant identiWcations were performed using Flora Iberica (Talavera et al. 1999–2000). Samples from Hungary (Jermy and Szentesi 2003), collected over a 17year period, were added to the present study as they were processed in the same conditions and identiWcations were checked by K.-W. Anton. The botanic nomenclature is mostly that of ILDIS (2005), except for some Iberian taxa which were named following Flora Iberica. Samples were composed of enough material to take into account occasionally low infestation rates (see Delobel and Delobel 2003). They were kept at room temperature for 6 months with regular checking and collection of emerging insects, which were dipped alive in 70% ethanol for identiWcation or 90% ethanol for molecular studies. The general list of samples, including precise locations, dates of collection
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Table 2 Host plant relationships between Genistoids and Bruchinae Section
Genus
Species
Samples
Thermopsideae
Anagyris Baptisia Genista
foetida australis corsica Xorida tinctoria pulchella scorpius sagittale pilosa monspessulana horridum junceum sessilifolium hirsutus spinescens albus austriacus villosus arboreus spinosa villosa scoparius striatus multiXorus nigricans oromediterraneus alpinum anagyroides angustifolius cosentinii luteus micranthus sp
4 1 2 1 52 1 5 1+2 2+4 5 1 9+8 3+2 3+16 1 2 17 4 2 2 6 10+3 1 1 30 4 1+1 5+8 6 1 1 5 3
Genista
G. pilosa Echinospartum Cytisus1 Cytisus2
Chamaespartium Genista Teline Echinospartum Spartium Cytisophyllum Cytisus
Cytisus Calicotome Cytisus
Laburnoides
Laburnum
Lupinus
Lupinus
Bruchid species
villosus (1)
villosus (2)
villosus (2) villosus (2), lividimanus (3) lividimanus (2), villosus (5+4) villosus (3+2), lividimanus (1) villosus (3+3), lividimanus (2)
lividimanus (3), villosus (2) lividimanus (1) lividimanus (2) lividimanus (2), villosus (2) lividimanus (9+1),villosus (2+3) lividimanus (1)
villosus (1) villosus (4+2) rubiginosus (1)
rubiginosus (1)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data. The following Genistoid species did not harbour any seed beetle (the number of samples is given between brackets): Section Adenocarpeae: Adenocarpus anisochilus (1); Section Phyllobotris: Genista anglica (2), germanica (2), hispanica (1), triacanthos (1), hirsuta (5); Section Spartocarpus: Genista spartioides (1), Retama monosperma (1), sphaerocarpa (2), Pterospartum tridentatum (1), Genista umbellata (1), Stauracanthus spectabilis (1), Ulex argenteus (1), australis(1), borgiae (1), erinaceus (1), europaeus (2), minor (2), parviXorus (4)
and infestation rates, is available upon request to the authors. European bruchid taxonomy is confused and partly unstable. In some instances, species identity is still in debate. A striking example is that of Bruchidius unicolor (Olivier), for which two conXicting neotypes were recently created (Borowiec 1988; Zampetti 2001). We used Borowiec’s (1988) revision of European bruchids as a basis for our identiWcation work. Anton’s (1998, 1999, 2001) major contributions to the European fauna were also essential for the identiWcation of some rare or little known species. In case of doubt, specimen identiWcation was conWrmed by K.-W. Anton. In several instances, types were studied (Delobel 2004). In all cases, series of males were dissected and their genitalia compared to identiWed material.
Results In the area under study, Bruchine larvae predate mostly upon Legume seeds; those Legumes all belong to the Faboideae clade, which is by far the most important clade in the area. Bruchinae attack the only two Faboideae subclades present in Europe (Fig. 1), even though they are phylogenetically distant: Genistoids s.l. and Hologalegina. Genistoids The Genistoid clade (Table 2) is represented in Europe by members of the core Genistoids (sensu Crisp et al. 2000) and more precisely by two tribes: Thermopsideae, with only one native (Anagyris foetida, a relict of
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Table 3 Host plant relationships between Robinioids and Bruchinae Section
Genus
Species
Samples
Anthyllis
Anthyllis vulneraria
barbajovis cytisoides hermanniae montana polycephala vulneraria circinnatus lotoides tetraphylla cornicina alpinus angustissimus conimbricensis conjugatus corniculatus creticus cytisoides edulis glaber maritimus ornithopodioides pedunculatus peregrinus preslii hirsutum pentaphyllum rectum compressus perpusillus pinnatus coronata glauca juncea minima repanda scorpioides ciliata comosa emerus multisiliquosa securidaca varia muricatus sulcatus vermiculatus
1 1 1 1 1 17+26 3 5 5 2 1 2 1 1 17+75 2 4 4 3 1+10 6 2 1 3 9 7 1 9 1 7 2 3 2 1 3 7 2 4 14+3 5 1 5+82 10 4 2
Hymenocarpos Tripodion OW Lotus
Lotus
Dorycnium
NW Lotus sl
Ornithopus
Coronilleae
Coronilla
Hippocrepis
Securigera Coronilleae sl
Scorpiurus
Bruchid species
poupillieri (8+2) bituberculatus (1) seminarius (2)
seminarius (1) seminarius (2) seminarius (3) seminarius (3) seminarius (1+5) seminarius (5) seminarius (1) seminarius (1)
pauper (6) pauper (4) pauper (1) borowieci (2) pauper (1), borowieci (1) pauper (2) pauper (2) pusillus (1) pusillus (11) seminarius (1) pusillus (1) pusillus (4+33) seminarius (7), taorminensis (2) seminarius (3), taorminensis (3) seminarius (1), taorminensis (1)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data
the Tertiary) and one introduced species (Baptisia australis) on one hand, and the large Cytiseae on the other. No bruchid was obtained from four samples of A. foetida, but Bruchidius villosus (F.) was obtained from cultivated B. australis. No bruchid could be reared from the single Portuguese sample of Adenocarpus. The 30 samples from the two sections Phyllobotrys and Spartocarpus (genera Ulex, Pterospartum, Retama, Stauracanthus and part of Genista) did not host any Bruchid. In the Genista section, only Genista tinctoria hosted Bruchids: 2 samples out of 52 produced
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Bruchidius villosus in Hungary (Jermy and Szentesi 2003). Section Genista pilosa (G. pilosa + Teline p.p.) hosted B. villosus and B. lividimanus (Gyll.). The related genera Cytisus, Spartium and Calicotome also hosted both species, often on the same plant specimen. The Laburnoides section of Cytiseae yielded only B. villosus. The wide genus Lupinus constitutes a very isolated section of Cytiseae; no Bruchid was obtained from any of the collected pods, but seeds collected on the ground around mature plants were infested by B. rubiginosus (Desbr.).
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Table 4 Host plant relationships between IRLClade (non-Vicioids) and Bruchinae Section
Genus
Species
Samples
Bruchid species
Hedysareae
Hedysarum
coronarium glomeratum spinosissimum aequidentata aliacmonia arenaria caput-galli humilis montana supina viciifolia alopecurus asper australis austriacus cicer clusianus contortuplicatus cymbaecarpos dasyanthus depressus drupaceus echinatus epiglottis exscapus glaux glycyphyllos hamosus incanus monspessulanus onobrychis pelecinus scorpioides sempervirens sinaicus stella suberosus tragacantha varius vesicarius lapponica pilosa baetica arborescens
2 1 1 4 1 1+6 10 1 1 1 1+7 1 3 1 4 1+28 1 1 2 1 4 1 2 1 4 1 1+62 10 1 9 2+20 8 1 1 1 3 2 3 2 1+3 1 7 4 1
gilvus (2)
Onobrychis
Astr. clade
Astragalus
Oxytropis Erophaca Colutea
gilvus (1) gilvus (1), olivaceus (1) poupillieri (1) lutescens (3)
gilvus (1), unicolor (1) varipes (1)
poecilus (1)
bernardi (1) caninus (1)
caninus (1) marginalis (1+24) caninus (8), poecilus (4) marginalis (6) varipes (7) caninus (1) poecilus (1) caninus (2), poecilus (1) caninus (1) varipes (1) marginalis (1), varipes (1) varipes (2)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data
Milletioids In Europe, only two monospeciWc genera (Psoraleae tribe) are present in this clade; Bituminaria bituminosa was sampled, with no bruchid obtained. Hologalegina clade This clade is divided in two sister subclades: Robinioids and the Inverted Repeat Lacking Clade (IRLClade), both containing genera hosting Bruchinae. In the
Robinioid subclade, Robinieae are represented by the introduced Robinia pseudoacacia from which no bruchid was obtained; genus Sesbania does not belong to the European Flora, but in Africa and Asia it is exploited by Bruchidius chloroticus (Dalman), and in Central and Western Africa by B. schoutedeni (Pic). All genera of Loteae (Table 3) hosted Bruchidius species, although in some genera a few species only were attacked, always at a low infestation level. Loteae can be further divided in several homogeneous groups (Allan et al. 2003), which are not fully resolved. ‘Old
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Table 5 Host plant relationships between Galegeae + Cicereae + Medicagoids and Bruchinae Section
Genus
Species
Samples
Bruchid species
Galegeae Cicereae Medicagoids
Galega Cicer Medicago
oYcinalis arietinum arabica arborea coronata disciformis intertexta littoralis lupulina marina minima murex muricoleptis orbicularis polymorpha praecox rigidula rugosa sativa truncatula turbinata
4+6 1 3 4 1 4 1 2 8 5 8 1 1 18 23 5 7 1 5 6 1
imbricornis (4+5)
nanus (1)
bimaculatus (1) bimaculatus (4), tibialis (1) calabrensis (1) bimaculatus (1) bimaculatus (3), nanus (11), tibialis (1) bimaculatus (4), tibialis (7) bimaculatus (3), tibialis (2) bimaculatus (3)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data. The following Medicagoid species did not harbour any seed beetle (the number of samples is given between brackets): Trigonella balansae (2), gladiata (4), graeca (1), monspeliaca (3), polyceratia (1), spruneriana (1). Melilotus indica (1), italicus (1), neapolitana (1), sp. (4). Ononis breviXora (1), minutissima (3), natrix (3), pubescens (1), pusilla (3), ramosissima (4) reclinata (1), repens (2), reuteri (1), sp. (3), spinosa (2), tridentata (1), variegata (1), viscosa (2)
World Lotus’ (Lotus plus Dorycnium) were predated upon by Bruchidius seminarius (L.). ‘New World Lotus’ include the Old World genus Ornithopus, which was attacked by Bruchidius pauper (Boh.), also found in Coronilleae seeds. In the Anthyllis group, A. vulneraria and its numerous subspecies were attacked by Bruchidius poupillieri (All.), Hymenocarpos circinnatus by Bruchidius bituberculatus Schils., a species never found on any other plant, and H. lotoides by B. seminarius. Coronilla seeds yielded only B. pauper (which was never found on other Coronilleae) and also Bruchidius borowieci Anton. On the other hand, Hippocrepis and Securigera shared Bruchidius pusillus (Germ.), whereas B. seminarius, already found on Lotus, was also obtained from Hippocrepis and Scorpiurus. In addition to B. pusillus and seminarius, Scorpiurus harboured, on the same samples, its own specialist B. taorminensis (Blanch.). The IRLClade Most European genera in this clade (Table 4) host seed beetles. Glycyrrhiza, a singular genus, former member of the polyphyletic Galegeae tribe, is in fact a sister group of all other European members of the IRLClade (Fig. 1). Its distribution in all temperate zones of the world is sustained by 20 species, some of them like G. glabra in cultivation for several centuries (North-
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Eastern Spain). In Hungary, G. echinata, a native species, is attacked by Bruchidius glycyrrhizae (Fahr.) whereas the introduced G. glabra is not. The sister group of Glycyrrhiza comprises two clades, one containing Hedysareae and the Astragalean subclade, the other one composed of Vicioids. In the Hedysareae, the genus Hedysarum is often heavily attacked, with up to 25% of the seeds harbouring bruchids when, on the contrary, Onobrychis is seldom attacked. This genus has fewer representatives in Western Europe than in Eastern Mediterranean and Central Asia, where several genera (Hedysarum, Onobrychis, Caragana) harbor numerous members of the B. unicolor group. Beside Paleoacanthoscelides gilvus (Gyl.), present on four diVerent species of the two genera, four Bruchidius species were identiWed, each on its own particular host species. The Astragalean subclade is represented by the gigantic genus Astragalus (2,000 species), the related Oxytropis, the monospeciWc Erophaca and Colutea. Obviously, the 182 samples collected can give only a faint idea of such an important group. About half of the plant species were found infested by a total of six species of Bruchidius. Vicioids constitute a very homogenous group. Two small genera (Galega and Cicer, Table 5) are the sister group of Medicagoids + Trifolium + Vicieae (Fig. 1). Galega, a genus with only six species in Eurasia and
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Table 6 Host plant relationships between Trifolium and Bruchinae Section
Genus
Species
Samples
Bruchid species
Trifolium
Trifolium
alpestre angulatum angustifolium arvense bocconei cherleri diVusum gemellum hirtum incarnatum lappaceum leucanthum ligusticum medium obscurum ochroleucon pallidum pannonicum phleoides pratense rubens scabrum smyrneum stellatum striatum repens fragiferum physodes resupinatum tomentosum vesiculosum subterraneum
1+11 1 16 4+3 2 6 1 2 1 1+3 6 2 1 2+22 1 1+4 1+1 4 4 13+16 1+17 3 1 10 2+6 10+12 11+3 3 2 4 1 2
varius (5)
T. repens Vesi+Misty
Trifolium Trifolium
Trichocephalum
Trifolium
martinezi (5), picipes(4), pygmaeus (5), sericatus(4) dispar (1), martinezi (1) annulicornis (1) varius (1) pygmaeus (2)
dispar (2), varius (2) picipes (1) picipes (1), pygmaeus (1)
pygmaeus (4) dispar (7+1), pygmaeus (9), sericatus (7), varius (9) sericatus (1), varius (5)
pygmaeus (7), sericatus (1) dispar (3), picipes (2), pygmaeus(2), sericatus (2) martinezi (1), varius (3) martinezi (2), varius (4) varius (2)
fulvicornis (1), sericatus (1) murinus (1)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data. The following Trifolium species did not harbour any seed beetle (the number of samples is given between brackets): Section Chromosemium: Trifolium boissieri (2), aureum (20), campestre (3+4), patens (3); Section Trifoliastrum: Trifolium alpinum (2), hybridum (6), nigrescens (1), montanum (6), retusum (1), glomeratum (6)
North Africa, formerly joined with Astragalus and Glycyrrhiza, is now clearly separated. Galega oYcinalis hosted a specialized species, Bruchidius imbricornis (Panz.). Cicer arietinum is less and less cultivated in Western Europe, and the only sample from an Andalusian Weld was uninfested; it may well have been treated with pesticides. Of the Medicagoids (Table 5), Trigonella, Melilotus and Ononis (24 species) did not harbor any bruchid. Ten Medicago species never yielded any bruchid, but eight species yielded three diVerent Bruchidius: B. bimaculatus (Ol.), B. nanus (Germ.) and B. tibialis (Boh.). Each of them was found in several Medicago species. Bruchidius calabrensis (Blanch.) was obtained only from M. murex. It must be noted that infestation levels were often very low in Medicago (10,750 seeds of M. orbicularis yielded 26 individuals of B. nanus and one of B. tibialis); the mean overall rate of infestation in infested samples was as low as 0.32%.
Of the Trifolium (Table 6), plants from Chromosemium and Trifoliastrum s. s. sections were never attacked by bruchids. T. repens is attacked by two species of Bruchidius, but it is no longer recognized as belonging to the Trifoliastrum section. Plants in the Trichocephalum section (T. subterraneum) bury their seeds in the soil, where they become infested by the specialist Bruchidius murinus (Boh.). The other species (sections Trifolium, Vesicularia and Mystillus) hosted eight diVerent Bruchidius with up to four species on the same plant species. Of the 30 species in these three sections, only 53% hosted Bruchids. The Vicieae tribe (Table 7), with its usually large seeds, was the only larval food plant of the genus Bruchus. Vicieae as a whole hosted 22 species of Bruchus, with often three or four species found in the same plant species. Infestation levels were high, always above 1% and often reaching 25%. Only 33 out of 27 Lathyrus and 9 out of 33 Vicia did not harbor any Bruchus. Some
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Table 7 Host plant relationships between Vicieae and Bruchinae Section
Genus
Species
Samples
Bruchid species
Lath.+ Lin.
Lathyrus
pannonicus angulatus digitatus sphaericus annuus cicera grandiXorus hirsutus latifolius odoratus sativus sylvestris tingitanus tuberosus setifolius linifolius niger occidentalis venetus vernus nissolia clymenum pratensis aphaca sp sativum altissima benghalensis cassubica cracca disperma dumetorum eriocarpa ervilia gracilis hirsuta incana monantha onobrychioides parviXora peregrina pisiformis pseudocracca pubescens sparsiXora tenuifolia tetrasperma villosa bithynica faba grandiXora hybrida lathyroides lutea melanops narbonensis pannonica sativa sepium culinaris ervoides nigricans
8 2 2 6+2 3 8 2 2+8 6+27 1+2 7 2+33 4 2+54 2 2 26 1 1 8 1+9 5 5+56 8+3 1 7+12 2 4 28 3+50 5 7 1 1 1 9+22 1 2 1 2 7 13 1 2 8 2+90 5+10 12+23 5 4+3 25 8 6+3 9 1 1+2 1+18 49+116 5+35 1 2 1
atomarius (4), viciae (3)
Lathyrus
Lathyrus
Orobastrum Orobus
Lathyrus Lathyrus
Nissolia Clymenum Pratenses Aphaca
Lathyrus Lathyrus Lathyrus Lathyrus
Pisum Vicilla
Pisum Vicia
Vicia
Vicia
Lens
viciae (2) viciae (4), tristiculus (4) pisorum (1), tristiculus (1) ruWmanus (1), tristiculus (3), luteicornis (1), tristis (2) aVinis (1) tristiculus (2+4) aVinis (3+13), atomarius (1), tristiculus (1) tristiculus (1+2) aVinis (1+15), tristiculus (1), atomarius (1) tristiculus (3) aVinis (1+12), tristiculus (1) dentipes (1) atomarius (5), viciae (4) atomarius (1) ruWmanus (1) atomarius (6) loti (2), tristiculus (1) brachialis (1), tristiculus (5) loti (5+5), aVinis (1), viciae (2) laticollis (3), tristiculus (1) ulicis (1) pisorum (6+5), tristiculus (1) ibericus (2) atomarius (3) libanensis (7), occidentalis (1+10), venustus (2+2) signaticornis (3), ibericus (1)
signaticornis (1) ibericus (1), ruWpes (1) ruWmanus (1) griseomaculatus (1) emarginatus (3), ruWmanus (1) atomarius (4) brachialis (1), atomarius (3) brachialis (1+8), libanensis (44), occidentalis (30), venustus (31) griseomaculatus (3), ruWpes (1) brachialis (7+8), ruWmanus (2), ruWpes (1), venustus (1) ruWmanus (2) ruWmanus (2) luteicornis (14) ruWmanus (6) ruWmanus (6) ruWmanus (1) brachialis (1), ruWmanus (13) brachialis (1), luteicornis (9+65), ruWpes (22) atomarius (5+13) lentis (1) signaticornis (1)
Bold Wgures identify samples collected by the authors, regular Wgures refer to Jermy and Szentesi (2003) data
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437
Fig. 2 Schematic male genital morphology of main Bruchidius species groups. a villosus group, b seminarius group, c unicolor group, d astragali group, e varius group, f cinerascens group, g tibialis group, h foveolatus group, i Paleoacanthoscelides gilvus group, j Bruchus
species were heavily sampled in diVerent geographic areas to ascertain their non-host status. Such was the case of Lathyrus sativus (7 samples), Vicia hirsuta (31 samples) and Vicia lathyroides (9 samples).
Discussion Research on the evolution of bruchid diets has long been hindered by generalized vagueness on the true nature of diets themselves. It is meaningful to observe that the exclusive (or nearly so—see Bruchus emarginatus All. on Tribulus terrestris: Delobel and Delobel 2005) link existing between genus Bruchus and tribe Viciae was unveiled only recently. As a matter of fact, based on old erroneous reports, Bruchus loti has long been considered as a predator of Lotus uliginosus seeds (e.g., Decelle 1989). On the other hand, the numerous tropical species still listed as Bruchus (Johnson 1981a; Udayagiri and Wahdi 1989) actually belong to the tribe Acanthoscelidini; most of them are probably associated with Mimosoideae (see for example Anton and Delobel 2003). We propose a reconsideration of the links between plants and bruchids on the basis of precise biological data. Seed beetle groups and their diets Bruchidius serraticornis group Two members of this group, B. quinqueguttatus and B. rubiginosus, diversiWed early in the history of European Bruchinae (Kergoat et al. 2005b); the group is probably the Wrst one to have adapted to Genistoids. B. rubiginosus is
unquestionably known only from lupine; host plants of other members of the group (B. quinqueguttatus, jocosus, meleagrinus, serraticornis, etc.) are unfortunately little known. B. quinqueguttatus (Ol.) and B. serraticornis (F.) were recorded (among other hosts) on Lupinus spp. in Israel (Anton et al. 1997). An exclusive relationship could well exist between genus Lupinus and the B. serraticornis group as a whole, but further biological data are needed. Bruchidius seminarius group The genital morphology of B. villosus and lividimanus (internal sac without spines, but with dense groups of thin spicules, compare Fig. 2a, b) leads us to treat these two species as distinct from the rest of the group. This is conWrmed by molecular data (Kergoat et al. 2004). The group composed of these two species will be referred to as B. villosus group. Polyphagy in the villosus group is high: villosus predates on 12 species belonging to seven diVerent sections of Genistoids, lividimanus on ten species in four sections of Genistoids. B. mulsanti belongs to this group because of its lack of spines in the internal sac; moreover, it is supposed to feed on seeds of Cytisus proliferus (Lukjanovitch and Ter-Minassian 1957). The seminarius group s.s. This group is associated with Robinioids. It is made up of very similar species, several of which were considered as sub-species or varieties until Anton’s 1998 revision. B. seminarius has the widest diet breadth as it utilizes four genera (14 species) in three diVerent sections; B. pusillus two genera (four species) in a single section; the other three species occupy a narrower niche: bituberculatus one
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single species, borowieci two species, and taorminensis three close species in a single genus. Bruchidius pauper group This has two members in the area, B. pauper and B. biguttatus. B. pauper predates upon seeds of two Robinioid genera belonging to diVerent sections: Ornithopus (two species) and Coronilla (four species). Following a host shift, B. biguttatus feeds in the capsules of several Cistaceae (two genera: Cistus and Halimium). Morphology is not very informative, but molecular data (Kergoat et al. 2004) show them as sister species. Bruchidius unicolor group The members of this group are usually diYcult to distinguish from each other because their morphologies are quite similar. The aedeagus is characterized by the presence of a pair of large and well sclerotized hinge sclerites; apex of lateral lobes is unmodiWed (Fig. 2c). In spite of its morphological homogeneity, the group exhibits a wide range of diets: B. poupillieri feeds in the seeds of the Robinioid Anthyllis vulneraria and, according to Jermy and Szentesi (2003), on Hedysareae (Onobrychis); B. unicolor, B. olivaceus and B. lutescens appear as strictly associated with tribe Hedysareae, each of them being associated with a diVerent species of Onobrychis. Some Western and Central Asian members of the group are associated with Hedysareae: B. convexicollis Lukj. with O. viciifolia and O. pulchella, B. onobrychidis with O. grandis (Lukjanovitch and TerMinassian 1957). B. cisti was obtained in Iraq from capsules of Helianthemum aegyptiacum (Decelle and Lodos 1989); H. nummularium and H. ovatum are mentioned as possible hosts of B. cisti in Europe (Decelle 1989; Anton 1994). Bruchidius astragali group Species in this group are exclusively associated with the Astragalean Clade. Although their external morphology is very similar to that of members of the varius group, their male genitalia is quite distinctive (Fig. 2d): the median lobe is stout, its dorsal valve ends in a point bearing dense setation, lateral lobes are widened apically. Moreover, they are clearly separated by molecular biology. B. varipes, which is an East European vicariant of B. marginalis, utilizes four species in two closely related genera, Oxytropis and Astragalus, B. caninus Wve species of Astragalus, B. marginalis three species, B. bernardi a single Astragalus. Even though B. poecilus feeds on four species of Astragalus, molecular data (Delobel et al. 2004) place this species close to the varius group; its male genitalia are typical of the varius group, not of the astragali group.
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Bruchidius varius, murinus and bimaculatus groups These three morphological groups deserve to be treated as a single one. They share a common male genital morphology, characterized by the following: median lobe elongated, lightly sclerotinized, internal sac without large spines, densely lined with tubercles in its proximal part, usually with small denticles distally; ventral valve rounded, ending in a more or less elongated pubescent beak; apex of lateral lobes modiWed (Fig. 2e). Molecular phylogenetics (Kergoat et al. 2004) conWrm the close relationship between varius and bimaculatus groups, data on the position of murinus are not available. We propose to identify the new species group as the Bruchidius bimaculatus group. Its members are linked with Vicioids (Galega + Medicagoids + Trifolium). Many species predate upon Trifolium seeds: B. varius and B. martinezi infest seven and three species, respectively, in three diVerent sections of Trifolium. B. picipes and B. dispar both predate on three species in a single section, B. annulicornis and B. fulvicornis only one species. It is worth mentioning that, due to the usually small size of Trifolium seeds, larvae in this group often cannot achieve their development in a single seed. During the course of their development, they migrate into a new seed, either within the same pod, or in a new pod. In the murinus group, B. murinus feeds in the single large seed of T. subterraneum (Trichocephalum section of Trifolium); B. calabrensis was found only in the seeds of M. murex, a Medicagoid. In the bimaculatus group, B. bimaculatus and B. nanus feed respectively in seven and two species of Medicago. B. imbricornis is morphologically similar to Trifolium-feeding species, but is found only on Galega oYcinalis. Bruchidius cinerascens group B. cinerascens is the sole member of its group. It feeds on various species in genus Eryngium (Apiaceae). Its aedeagus shows some similarity with that in the previous group (Fig. 2f): elongated median lobe with rounded ventral valve ending in a long curved beak, absence of spines in the internal sac, lateral lobes apically modiWed. The characteristically elongated body shape may be related with pupation in host plant stems. Bruchidius tibialis group The external morphology of B. tibialis and B. longulus has much in common with the varius group. Male genital morphology is, however, quite distinctive, with lateral lobes strongly modiWed and tegminal strut keeled (Fig. 2g). We found B. tibialis on four species of Medicago. We failed to identify the host of B. longulus; it was, however, obtained in Western Asia (Decelle and Lodos 1989) from several
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Trigonella spp., which conWrms a strong aYnity with the varius group. An old report (HoVmann 1945), according to which B. longulus feeds on Astragalus monspessulanus, seems either a misinterpretation or a rare occurrence. Bruchidius foveolatus group In the area under study, this group comprises B. foveolatus and two small-sized species feeding on Trifolium: B. pygmaeus (seven species in one section of Trifolium) and B. sericatus (four species in two sections). Male genitalia (Fig. 2h) are characterized by the presence in the internal sac of a pair of elongated hinge sclerites and two strands of strongly sclerotized denticles; lateral lobes are wide, deeply cleft, and their apex is slightly modiWed. Contrary to members of the varius group, their larvae can complete their development in a single seed. Even though it is very common in collections, B. foveolatus has no satisfactorily identiWed host plant; according to available bibliography, its host could be one or several of the following species: Cytisus scoparius (HoVmann 1945), Spartium junceum (Decelle and Lodos 1989), Genista fasselata (Anton et al. 1997). We were, however, unable to obtain B. foveolatus from any of these Genistoids. Paleoacanthoscelides gilvus This species belongs to a monospeciWc group, which is the sister group of the genus Bruchus (Kergoat et al. 2004). Male genitalia have the same general shape as found in Bruchus, with a Xat elongated basal hood, but the tegminal strut has a long keel, and lateral lobes are fused almost to apex (Fig. 2i). Its host plants belong to the two genera of Hedysareae, with two species in each genus. Tribe Bruchini Genus Bruchus (Table 2) is the sole member of this tribe. External morphology is quite distinctive, with spiny pronotal sides and modiWed mid tibiae in males; male genitalia (Fig. 2j) bear some similarity with P. gilvus, but the tegminal strut is without keel, and lateral lobes are deeply cleft. Borowiec’s species groups can be reorganized according to the two main phylogenetic clades identiWed by molecular analysis (Kergoat et al. 2004): aVinis, atomarius, loti, and ruWpes groups are united in a single aVinis clade, whereas groups brachialis, pisorum, and tristis are united in the brachialis clade. In the aVinis clade, four species (B. aVinis Fröl., viciae Ol., loti Payk., and dentipes Baudi) are exclusive Lathyrus feeders, Wve species (Borowiec’s ruWpes group: B. griseomaculatus Gyll., occidentalis Lukj., libanensis Zamp., luteicornis Ill., and ruWpes Herbst) are exclusive Vicia feeders, and two species (B. atomarius (L.) and ruWmanus Boh.) predate
439
upon species belonging to both genera. The situation is similar in clade brachialis, where four species (B. tristiculus Fahr., tristis Boh., laticollis Boh., and pisorum (L.)) are exclusive Lathyrus feeders, Wve species exclusive Vicia feeders (B. ibericus Anton, venustus Fahr., emarginatus All., lentis Fröl., and signaticornis Gyll.) whereas one species (brachialis Fahr.) Wnds its hosts in both genera. Species with a wider diet breadth may thus be found in both clades. Most species are, however, specialized: Wve species of clade aVinis and seven species of clade brachialis Wnd their hosts in a single section. Bruchus phylogeny (Kergoat et al. 2006) reveals that shifts from Lathyrus to Vicia and vice versa have occurred several times independently in both Bruchus clades. It may be added that, considering the similarity of morphologies and diets in several groups of Bruchus, partial interfertility (Thompson 1998) is plausible; it could explain variations and partial overlap in external as well as genital morphology observed among species. Diet breadth The number of host species, genera and sections used by each seed beetle, as given in Tables 2, 3, 4, 5 and 6 and summarized above, gives only a rough indication of the actual polyphagy level of European beetles because it does not take into account the relationships between plant species. Computation of polyphagy indices (Symons and Beccaloni 1999) is a way of solving this problem. Unfortunately, such analysis could not be performed for lack of detailed host plant phylogenetic hypotheses. Even in the absence of exact measurement, the diet of European seed beetles unequivocally appears as highly specialized: out of 55 species with identiWed hosts, 46 feed on plants belonging to one single genus. Only a few Western European bruchines may be described as polyphagous or oligophagous; these species predate on Genistoid and Robinioid seeds and belong to the B. villosus and B. seminarius groups. B. villosus predates upon the seeds of 12 species belonging to seven Genistoid sections, B. lividimanus on 10 species in three sections; B. seminarius on 14 species in three sections. A further six species use hosts belonging to two or three diVerent genera. Actually these seed beetles are not true generalists, but are specialized on a small number of related hosts, in much the same way as butterXies studied by Nylin and Janz (1998). There is no example in Western European bruchids of species using a large array of hosts, ranging over diVerent subfamilies of Fabaceae, as in the New World genus Stator (Morse and Farrell 2005).
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Patterns of Bruchid–plant interactions Western European representatives of the sub-family Bruchinae are characterized by a strong taxonomic conservatism. B. cinerascens and B. biguttatus (and possibly B. cisti) represent exceptions to the general rule: they have shifted to hosts outside Leguminosae. B. poecilus has shifted from Trifolium to the Astragalean clade. On the other hand, the development of wild Bruchus emarginatus on Tribulus terrestris (Zygophyllaceae) (Delobel and Delobel 2003) shows the potential of a highly specialized species to experience major changes in host taxa preference (see also Ehrlich and Raven 1964; Farrell and Mitter 1993). The defences of several plant clades were overrun twice independently by unrelated bruchid groups: Hedysareae were invaded once by Paleoacanthoscelides gilvus, sole member of a group that did not experience any subsequent radiation, and once by members of the B. unicolor group, which experienced an important radiation on Onobrychis. Astragaleae experienced two independent invasions: once by the astragali group, with subsequent radiation, and once by B. poecilus. Similarly, Loteae harbour bruchids belonging to three diVerent species groups, seminarius, pauper and bituberculatus. B. seminarius is adapted to numerous sections of Loteae; it does not feed in Coronilla and Ornithopus, which are fed upon by one species of another group, B. pauper. All other species in the group are specialized on a single or a few very close plant species. It may be noted that Securigera varia and Hippocrepis emerus, two Coronilleae formerly included in genus Coronilla until Lassen (1989) removed them, do not harbor B. pauper as do other members of genus Coronilla, but B. pusillus instead. This phenomenon of apparent exclusion is yet to be explained. It must be emphasized that, during the process of multiple infestation, the most ancient bruchid clades did not always attack plants belonging to the oldest clades. Indeed, lupines, which belong to Genistoids, the most ancient Faboideae in Western Europe, are infested by B. rubiginosus, a member of the ancient B. serraticornis species group. But the majority of Genistoids are predated upon by members of the derived B. villosus group. This is a new demonstration of the lack of congruence between current phylogenies of Bruchinae and their host plants. It has been hypothesized that plant chemical compounds play a major role in bruchid speciation (Kergoat et al. 2005a), and we may suppose for instance that alkaloids have prevented many bruchid species from developing on Genistoids. But at the moment there is no explanation why Cytisus spp. are
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attacked while most Genista and all Ulex are not, when they share most secondary compounds, grow in the same areas and ripen their seeds in the same time. Not only the nature of plant secondary compounds (for example, cytisin), but also their concentration and changing localization as a function of physiological stage, may help to shed light on this infestation pattern. A most careful study, taking into account small diVerences in chemical structure and concentration between plant species and even populations, is however needed. At the same time, advances in the knowledge of proteins involved in plant toxicity open up wide areas in the study of plant-insect interactions (Sales et al. 2000). Evidence of the role of alpha-amylase inhibitors in the speciWcity of bruchid–legume interactions (Schroeder et al. 1995) emphasizes the activity of small-sized proteins. The classic model of “escape and radiation” predicts that, after having bypassed the chemical barrier of resistance of a plant, an insect can gain access to most of the plant’s relatives and then radiate (Gillon et al. 1992; Nylin and Janz 1998). The above-mentioned examples of B. poecilus, P. gilvus and B. bituberculatus show that this is not always the case. Szentesi et al. (1996) demonstrated the existence of multiple infestation by Bruchus species in three species of Vicia; the present study shows that this is actually the case of almost all Vicieae. The genus Bruchus as a whole is morphologically very homogeneous, which could indicate that only one shift to Vicieae occurred, followed by intense radiation on genera Vicia and Lathyrus. Biogeography may partly explain not only this radiation, but also the extant co-occurrence of several closely related species on the same plant. Indeed, the last Ice Age has fragmented European Xoras and faunas, leading to allopatric evolution of plants and insects; a rapid postglacial colonization has allowed refugial genomes from diVerent southern shelters to regain sympatry (see Hewitt 1999). A few legume species, however, completely escape seed beetle infestation, and in particular V. hirsuta: bruchid eggs are laid on its pods, but adult emergence does not occur (Szentesi et al. 1996). It is one of the few Vicieae that produce and store cyanogenic glycosides (Hegnauer and Hegnauer 2001). As seeds of bruchid-infested Vicieae are free from cyanogenic compounds, it is tempting to relate the infestation pattern to this observed correlation. Some populations of V. sativa and its subspecies produce cyanogenic glycosides, some do not; part of our V. sativa samples were found infested by three diVerent species of Bruchus, part were uninfested. Thompson (1988) stressed the importance of nonchemical factors in insect-plant interactions (ecology of host plants, role of predators and parasites, etc.). The
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present study reveals the role of behavioural adaptation in broadening host spectra. Such is the case of bruchids predating on Trifolium seeds: they have adopted two distinct strategies, corresponding to two distinct species groups. Members of the pygmaeus group complete their development inside a single seed, thus promoting a size reduction of these species, whereas members of the varius group often migrate from one pod to another through an unusual behaviour of third or fourth instar larvae. They spin a web between neighbouring pods, allowing additional seeds to be fed on, as Wrst described by HoVmann (1945). Physical characteristics of the capitulum therefore play an important part in Trifolium selection. Species in section Chromosemium bear very small seeds (less than 1 mg) in singleseeded pods borne on long peduncles and are not adapted to development of any Bruchidius species. B. murinus predates upon seeds of T. subterraneum, a species with unusually large seeds that are buried in the soil before maturity. It belongs to a clade diVerent from other Trifolium feeders, which may indicate that adaptation to egg-laying on underground seeds is largely behavioural. Other soil-burying Leguminosae are known to have low chemical defences (Gillon et al. 1992) and harbour seed beetles with particular behaviours, like Callosobruchus subinnotatus (Pic) in Western Africa. The pod wall of Lupinus is known to be rich in highly noxious compounds such as anagyrin and quinolizidine alkaloids, present in the seed and pod wall (Keeler et al. 1976). This may protect lupines from most Bruchid species. B. rubiginosus has developed a strategy that enables females to oviposit on fallen seeds; such a strategy does not protect their progeny from these alkaloids but may act as a defence against the high levels of other toxic compounds abundant in the pod wall. This and other behavioural adaptations have been described in various New World species (Johnson 1981b). Conclusion A certain level of host conservatism prevails among West European Bruchinae: as in most phytophagous insects, related species usually feed on related plants (Farrell and Sequeira 2004). Ehrlich and Raven’s (1964) model of coevolution as understood by Janzen (1980) or Futuyma (1983) (reciprocal adaptations of interacting lines of insects and plants; see Nylin and Janz 1998) appears, however, largely inadequate in bruchids. Radiative speciation on a pre-existing background of host taxa may be considered as a highly plausible hypothesis in bruchids, as it is in other insects
441
(Janz and Nylin 1998). At a time when Legume and bruchid phylogenetic studies were only in their infancy, several authors came to much the same conclusion: Jermy (1984) developed the concept of “sequential evolution”; Johnson (1990) noted that coevolutionary evidence in bruchids was “correlative.” Jermy and Szentesi (2003) demonstrated in Hungarian Bruchinae and Morse and Farrell (2005) in New World Stator that a strict bruchid–plant coevolutionary model was not the most appropriate to describe biological data. It is also legitimate to consider that the extraordinary variety of biotic and non-biotic factors potentially interacting with a plant population precludes any kind of subordination of plants to a single one of these factors. The hypothesis of radiative adaptation, once again brought to light in the present study, is not conXicting with preliminary evaluations of periods of appearance of Bruchinae and Faboideae. Data are, however, too scanty to draw deWnite conclusions: Genistoids are Wrst recorded 50–55 Mya, the IRLClade 39 Mya (Lavin et al. 2005). The oldest fossil record of Bruchidae is 79 Mya; it was probably a palm-feeding bruchid belonging to the primitive subfamily Pachymerinae, and taxa from the Florissant shales in the U.S.A., about 35 Mya, probably belong to the same guild of palm predators (Kingsolver 1965; Poinar 2005). There is unfortunately no fossil record of the derived clades of Legume seed predators. Future progress should involve robust phylogenetic reconstruction based on population sampling (Barraclough and Nee 2001) throughout the Palaearctic domain. Such reconstruction is likely to provide strong hypotheses on factors associated with cladogenetic events.
References Allan GJ, Zimmer EA, Wagner WL, SokoloV DD (2003) Molecular phylogenetic analyses of tribe Loteae (Leguminosae): implications for classiWcation and biogeography. Adv Legume Syst 10:371–393 Asmussen CB, Liston A (1998) Chloroplast characters, phylogeny, and classiWcation of Lathyrus. Am J Bot 85:387–401 Anton KW (1994) Ergänzung und Berichtigungen zu FreudeHarde-Lohse “Die Käfer Mitteleuropas” Band 10 (1981). 89. Familie: Bruchidae. Die Käfer Mitteleuropas 14, 3: 143–151. Supplementband. Goecke, Evers Verlag, Krefeld Anton KW (1998) Revision of the genus Bruchidius. Part I: The B. seminarius Group (Coleoptera: Bruchidae). Stuttg Beitr Naturkunde A Biol 573:1–13 Anton KW (1999) Two new species of the brachialis group from the Mediterranean region. Linz Biol Beitr 31:655–660 Anton KW (2001) Bemerkungen zur Faunistik und Taxonomie mitteleuropäischer Samenkäfer (Coleoptera: Bruchidae). Folia Entomol Hung 62:43–49
123
442 Anton KW, Delobel A (2003) African species of the Bruchidius centromaculatus group with “eyed” female pygidium (Coleoptera: Bruchidae: Bruchinae). Genus 14:159–190 Anton KW, Halperin J, Calderon M (1997) An annotated list of the Bruchidae (Coleoptera) of Israel and adjacent areas. Isr J Entomol 31: 59–96 Badr A, El Shazly H, El Rabey H, Watson L (2002a) Systematic relationships in Lathyrus sec. Lathyrus (Fabaceae) based on ampliWed fragment length polymorphism (AFLP) data. Can J Bot 80:962–969 Badr A, Sayed-Ahmed H, Shanshouri A, Watson LE (2002b) Ancestors of white clover (Trifolium repens L.) as revealed by isoenzyme polymorphism. Theor Appl Genet 106:143– 148 Barraclough TG, Nee S (2001) Phylogenetics and speciation. Trends Ecol Evol 16:391–399 Bena G, Prosperi JM, Lejeune B, Olivieri I (1998) Evolution of annual species of the genus Medicago: a molecular phylogenetic approach. Mol Phylogenet Evol 9:552–559 Borowiec L (1988) Bruchidae—Strakowce (Insecta: Coleoptera). Fauna Polski. Fauna Poloniae, 11, Polska, PWN, Warszawa, 226 p Borowiec L, Anton KW (1993) Materials to the knowledge of seed-beetles of the Mediterranean subregion. Ann Upper Silesian Mus Bytom Entomol 4:99–152 Center TD, Johnson CD (1976) Host plants and parasites of some Arizona seed-feeding insects. Ann Entomol Soc Am 69:195– 201 Crisp MD, Gilmore S, van Wyk BE (2000) Molecular phylogenesis of the Genistoid tribes of papilionid Legumes. Adv Legume Syst 9:249–276 Cubas P, Pardo C, Tahiri H (2002) Molecular approach to the phylogeny and systematics of Cytisus (Leguminoseae) and related genera based on nucleotid sequences of of nrDNA (ITS region) and cpDNA (trnL-trnF intergeneric spacer). Plant Syst Evol 233:223–242 Decelle J (1989) Les Bruchidae (Coleoptera) de Belgique. In: Wouters K, Baert L (eds) Invertébrés de Belgique. C.R. symposium on international ‘Invertébrés de Belgique’, Bruxelles, Institut Royal des Sciences nbaturelles de Belgique, 468 p Decelle J, Lodos N (1989) Contribution to the study of Legume weevils of Turkey (Coleoptera: Bruchidae). Bull Ann Soc R Belge Entomol 125:163–212 Delobel A, Delobel B (2003) Les plantes hôtes des bruches (Coleoptera Bruchidae) de la faune de France, une analyse critique. Bull Mens Soc Linn Lyon 72:199–221 Delobel A (2004) Les types de Bruchidius décrits par Emile Blanchard (Coleoptera, Bruchidae). Rev Fr Entomol 26:165–173 Delobel B, Delobel A (2005) Les plantes hôtes des bruches (Coleoptera Bruchidae): données nouvelles et corrections. Bull Mens Soc Linn Lyon 74:277–291 Delobel A, Anton KW, Kergoat GJ (2004) New data on European Astragalus-feeding Bruchidius, with the description of a new species from Southern Italy (Coleoptera: Bruchidae: Bruchinae). Genus 15:173–185 Ehrlich PR, Raven PH (1964) ButterXies and plants: a study in coevolution. Evolution 18:586–608 Farrell BD, Mitter C (1993) Phylogenetic determinants of insect plant community diversity. In: Ricklefs RE, Schuter D (eds) Species diversity, historical and geographical perspectives, pp 253–266 Farrell BD, Sequeira AS (2004) Evolutionary rates in the adaptive radiation of beetles on plants. Evolution 58:1984–2004 Futuyma DJ (1983) Selective factors in the evolution of host choice by phytophagous insects. In: Ahmad S (ed) Herbivorous insects. Academic, New York, pp 227–244
123
Oecologia (2006) 149:428–443 Gillon Y, Rasplus JY, Boughdad A, Mainguet AM (1992) Utilisation des graines de Légumineuses par un peuplement de Bruchidae et d’Anthribidae en zone de mosaïque forêt-savane (Lamto: Côte-d’Ivoire). J Zool Afr 106:421–443 Hegnauer R, Hegnauer M (2001) Chemotaxonomie der PXanzen. Band11 b-2. Leguminosae. Teil 3. Birkhauser, Basel Hewitt GM (1999) Post-glacial re-colonization of European biota. Biol J Linn Soc 68:87–112 HoVmann A (1945) Coléoptères Bruchidae et Anthribidae. Faune de France 44, Lechevalier, Paris ILDIS (2005) International legume database and infornation service. Legume Web. http://www.ildis.org. Cited 12 Oct 2005 Janz N, Nylin S (1998) ButterXies and plants: a phylogenetic study. Evolution 52:486–502 Janzen JH (1980) SpeciWcity of seed-attacking beetles in a Costa Rican deciduous forest. J Ecol 68:929–952 Jermy T (1984) Evolution of insect/plant relationships. Am Nat 124:609–630 Jermy T, Szentesi A (2003) Evolutionary aspects of host plant specialisation—a study on bruchids (Coleoptera: Bruchidae). Oikos 101:196–204 Johnson CD (1981a) Seed beetle host speciWcity and the systematics of the leguminosae. Adv Legume Syst 2:995–1027 Johnson CD (1981b) Interactions between bruchid (Coleoptera) feeding guilds and behavioural patterns of pods of the leguminosae. Environ Entomol 10:249–253 Johnson CD (1990) Coevolution of Bruchidae and their hosts: evidence, conjecture, and conclusions. In: Fujii K, Johnson CD, Gatehouse AG, Mitchell RD, YoshidaT (eds) Bruchids and legumes: economics, ecology and coevolution. Kluwer, Netherlands, pp 181–188 Johnson CD, Kingsolver JM (1976) Systematics of Stator of North and Central America (Coleoptera: Bruchidae). U.S.D.A. Technical Bulletin 1537 Keeler RE, Cronin EH, Shupe JL (1976) Lupina alkaloids from teratogenic and nonteratogenic lupines. IV. Concentration of total alkaloids, individual major alkaloids and teratogenic anagyrin as a function of plant part and stage growth and their relationship to cooked calf disease. J Toxicol Environ Health 1:899–908 Kenicer GJ, Kajita T, Pennington RT, Murata J (2005) Systematics and biogeography of Lathyrus based on internal transcribed spacer and cpDNA sequence data. Am J Bot 92:1199–1209 Kergoat GJ, Delobel A, Silvain JF (2004) Phylogeny and hostspeciWcity of European seed beetles (Coleoptera, Bruchidae), new insights from molecular and ecological data. Mol Phylogenet Evol 32:855–865 Kergoat GJ, Delobel A, Fediere G, Le Ru B, Silvain JF (2005a) Both host-plant phylogeny and chemistry have shaped the African seed-beetle radiation. Mol Phylogenet Evol 35:602– 611 Kergoat GJ, Alvarez N, Hossaert-McKey M, Faure N, Silvain JF (2005b) Evidence for parallel evolution in the two largest seed-beetle genera (Coleoptera: Bruchidae). Mol Ecol 14:4003–4021 Kergoat GJ, Silvain JF, Delobel A, Tuda M, Anton KW (2006) DeWning the hierachical limits of taxonomic conservatism in phytophagous insects: molecular systematics and host-plant use in the seed-beetle genus Bruchus Linnaeus (Coleoptera: Chrysomelidae: Bruchinae) (in press) Kingsolver JM (1965) A new fossil bruchid genus and its relationships to modern genera (Coleoptera: Bruchidae: Pachymerinae). Coleopt Bull 19:25–30 Kupicha FK (1976) The infrageneric structure of Vicia. Notes R Gard Edinburgh 34:287–326
Oecologia (2006) 149:428–443 Kupicha FK (1983) The infrageneric structure of Lathyrus. Notes R Gard Edinburgh 41:209–244 Lassen P (1989) A new delimitation of the genera Coronilla, Hippocrepis and Securigera (Fabaceae). Willdenowia 19:49–62 Lavin M, Herendeen PS, Wojciechowski MF (2005) Evolutionary rates analysis of Leguminosae implicates a rapid diversiWcation of lineages during the tertiary. Syst Biol 54:575–594 Lingafelter SW, Pakaluk J (1997) Forum: comments on the bruchine Chrysomelidae. Chrysomela 33:3–4 Lukjanovitch FK, Ter-Minassian ME (1957) Zuki-zernovski (Bruchidae). Fauna SSR, Zestkokrylye, 24 1. Zoologiceskii Institut Akademii Nauk SSSR, NS 67:1–209 Morimoto K (1990) A synopsis of the bruchid fauna of Japan. Ser Entomol 46:131–140 Morse GE, Farrell BD (2005) Ecological and evolutionary diversiWcation of the seed beetle genus Stator (Coleoptera: Chrysomelidae: Bruchinae). Evolution 59:1315–1333 Nanni L, Ferradini N, TaVetani F, Papa R (2004) Molecular phylogeny of Anthyllis spp. Plant Biol 6:1–11 Nylin S, Janz N (1998) The ecology and evolution of host plant range: butterXies as a model group. In: OlV H, Brown VK, Drent RH (eds) Herbivores: between plants and predators. Blackwell, Oxford, pp 31–54 Pardo C, Cubas P, Tahiri H (2004) Molecular phylogeny and systematics of Genista (Leguminoseae) and related genera based on nucleotide sequences of nrDNA (ITS region) and cpDNA (trnL-trnF intergeneric spacer). Plant Syst Evol 244:93–119 Poinar G Jr (2005) A cretaceous palm bruchid, Mesopachymerus antiqua n. gen., n. sp. (Coleoptera: Bruchidae: Pachymerini) and biogeographical implications. Proc Entomol Soc Wash 107:392–397 Polhill RM (1981) Loteae, Coronilleae. Adv Legume Syst 1:371– 374 Sales MP, Gerhardt IR, Grossi-de-Sa MF, Xavier-Filho J (2000) Do legume storage proteins play a role in defending seeds against Bruchids? Plant Physiol 124:515–522 Schroeder HE, Gollash S, Moore A, Tabe LM, Craig S, Hardie DC, Chrispeels MJ, Spencer D, Higgins TJV (1995) Bean alpha-amylase inhibitors confer resistance to the pea weevil (Bruchus pisorum) in transgenic peas (Pisum sativum). Plant Physiol 107:1233–1239 Small E. (1987) Generic changes in Trifolieae subtribe Trigonellineae. Adv Legume Syst 3:169–181 Southgate BJ (1979) Biology of the Bruchidae. Annu Rev Entomol 24:449–473 Steele KP, Wojciechowski MF (2003) Phylogenetic analysis of tribes Trifolieae an Vicieae based on sequences of the plastid
443 gene matK (Papilionoideae: Leguminosae). Adv Legume Syst 10:355–370 Symons FB, Beccaloni GW (1999) Phylogenetic indices for measuring the diet breadths of phytophagous insects. Oecologia 119:427–434 Szentesi Á, Jermy T, Takács V (1996) Niche relations in Viciainhabiting Bruchus spp. Entomol Exp Appl 80:152–155 Talavera S, Aedo C, Castroviejo S, Romero C, Sáez L, Salgueiro FJ, Velayos M (1999–2000) LXXXVIII. Leguminosae. In: Castroviejo S (ed) Flora Iberica, real Jardin Botanico. CSIC, Madrid Thompson JN (1988) Coevolution and alternative hypotheses on insect/plant interactions. Ecology 69:893–895 Thompson JN (1998) The evolution of diet breadth: monophagy and polyphagy in swallowtail butterXies. J Evol Biol 11:563– 578 Tuda M, Chou LY, Niyomdham C, Buranapanichpan S, Tateishi Y (2005) Ecological factors associated with pest status in Callosobruchus (Coleoptera: Bruchidae): high host speciWcity of non-pests to Cajaninae (Fabaceae). J Stored Prod Res 41:31–45 Udayagiri S, Wahdi SR (1989) Catalog of Bruchidae. Mem Am Entomol Inst 45:1–301 Watson LE, Sayed-Ahmed H, Badr A (2000) Molecular phylogeny of old world Trifolium based on plastid and nuclear markers. Plant Syst Evol 224:153–171 Wendt H (1978) Die Bruchiden-Typen der Koleopteran-Sammlung des Zoologischen Museums Berlin. Mitt Zool Mus Berl 54:353–367 Wendt H (1992) Beitrag zur Bruchiden-Fauna der Balearen (Coleoptera, Chrysomeloidea). Dtsch Entomol Z 39:117– 122 Wojciechowski MF (2003) Reconstructing the phylogeny of legumes (Leguminosae): an early 21st century perspective. Adv Legume Syst 10:5–35 Wojciechowski MF, Sanderson MJ, Steele KP, Liston A (2000) Molecular phylogeny of the “temperate herbaceous tribes” of papilionoid legumes: a supertree approach. Adv Legume Syst 9:277–298 Wojciechowski MF, Lavin M, Sanderson MJ (2004) A phylogeny of Legumes (Leguminosae) based on analysis of the plastid MPATK gene resolves many well-supported subclades within the family. Am J Bot 91:1846–1862 Zampetti MF (2001) Bruchidius unicolor (Olivier, 1795) new neotypus proposed (Coleoptera, Bruchidae). Mus Reg Sci Nat Boll 18:107–114
123
