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Biology and Evolution of Adelgidae

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Biology and Evolution of Adelgidae ANRV297-EN52-16 ARI 21 November 2006 10:26 Biology and Evolution of Adelgidae Nathan P. Havill1 and Robert G. Foottit2 1Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520; email: [email protected] 2Agriculture and Agri-Food Canada, Eastern Cereal and Oilseeds Research Centre, Ottawa, ON K1A 0C6, Canada; email: [email protected] Annu. Rev. Entomol. 2007. 52:325–49 Key Words The Annual Review of Entomology is online at Aphidoidea, complex life cycle, cyclical parthenogenesis, ento.annualreviews.org plant-insect interactions This article’s doi: 10.1146/annurev.ento.52.110405.091303 Abstract Copyright c 2007 by Annual Reviews. The Adelgidae form a small clade of insects within the Aphidoidea All rights reserved (Hemiptera) that includes some of the most destructive introduced by Agriculture & Agri-Food Canada on 09/05/08. For personal use only. 0066-4170/07/0107-0325$20.00 pest species threatening North American forest ecosystems. De- spite their importance, little is known about their evolutionary his- Annu. Rev. Entomol. 2007.52:325-349. Downloaded from arjournals.annualreviews.org tory and their taxonomy remains unresolved. Adelgids are cyclically parthenogenetic and exhibit multigeneration complex life cycles. They can be holocyclic, with a sexual generation and host alterna- tion, or anholocyclic, entirely asexual and without host alternation. We discuss adelgid behavior and ecology, emphasizing plant-insect interactions, and we explore ways that the biogeographic history of their host plants may have affected adelgid phylogeny and evolution of adelgid life cycles. Finally, we highlight several areas in which ad- ditional research into speciation, population genetics, multitrophic interactions, and life-history evolution would improve our under- standing of adelgid biology and evolution. 325 ANRV297-EN52-16 ARI 21 November 2006 10:26 Two phenomena in the natural history of chermes twentieth century, interest in adelgids peaked [ = adelgids] are especially striking; the again. Eichhorn (45, 46) discussed popula- parthenogenesis and the polymorphism: both of tion dynamics and predator-prey interactions. them attain such a high degree here as nowhere Steffan (144, 145) studied systematics, cytol- else in the animal kingdom. N.A. Cholodkovsky, ogy, and life cycle evolution. Inouye (81) de- 1915 (29) scribed the adelgid fauna in Japan, as did Carter (25) in Britain. In recent decades, research on adelgids INTRODUCTION has focused mainly on two species, balsam Adelgids (Hemiptera: Aphidoidea: Adelgi- woolly adelgid, Adelges piceae (69), and hem- dae), like their closest relatives, phylloxer- lock woolly adelgid, A. tsugae (103). They ans (Phylloxeridae) and aphids (Aphididae), were introduced into North America from exhibit cyclical parthenogenesis and have Europe (60) and Japan (76), respectively, and complex, multigeneration, polymorphic life are serious threats to forest ecosystems. Re- cycles. The Adelgidae and Phylloxeridae are cent research has therefore emphasized basic distinguished from the Aphididae by the ab- biology, plant-insect interactions, and poten- sence of siphunculi and the retention of the tial biological control organisms to inform ef- ancestral trait of oviparity in all generations forts to manage these two species. In this re- (78). While phylloxerans and many aphids view, we give an overview of adelgid biology feed on angiosperms, adelgids feed only on and systematics and discuss recent advances in certain genera in the Pinaceae, retaining their understanding their evolutionary history. In ancestral relationship with gymnosperms (78, particular, we focus on the evolution of adel- 157). gid life cycles and host plant use. By emphasiz- Adelgids, like their host plants, are en- ing patterns across the whole family, we hope demic to Northern Hemisphere boreal and to stimulate research on this unique group of temperate environments. Despite the broad insects, to inform control programs of current geographic distribution of their host plants, adelgid pest species, and to help prevent other there are surprisingly few adelgid species: species from becoming pests in the future. Fewer than 70 have been described in the en- tire family (15, 124, 145) (Table 1). However, there is considerable taxonomic uncertainty. THE ADELGID HOLOCYCLE Several described species may not represent In cyclically parthenogenetic organisms, a unique taxa but are actually different morpho- holocyclic species or lineage is one that in- logical forms of the same species found on cludes a sexual generation in its life cycle. by Agriculture & Agri-Food Canada on 09/05/08. For personal use only. different host plants (15). It also is likely that Life cycles that do not include a sexual gen- cryptic species have yet to be described (76). eration are termed anholocyclic. Five gener- Annu. Rev. Entomol. 2007.52:325-349. Downloaded from arjournals.annualreviews.org Work on adelgid biology and systemat- ations make up the typical adelgid holocycle ics has a long and rich history. After cycli- (Figure 1, center). Three are produced on the cal parthenogenesis and host alternation were primary host, where sexual reproduction and discovered in adelgids between 1887 and gall formation occur; two are produced on the 1889 (17, 18, 27, 42), a lively dialogue secondary host that supports a series of asexual in the scientific literature established their generations. The entire cycle takes two years natural history, life cycle terminology, and to complete. Spruce (Picea spp.) is always the the morphological characters used in taxon- primary host and another conifer genus (Abies, omy, culminating in monographs by Cholod- Larix, Pseudotsuga, Tsuga,orPinus) is always kovsky (28) in Russia, Borner¨ (22) in Ger- the secondary host. Adelgids are highly host many, Marchal (97) in France, and Annand specific: A given species can survive and re- (4) in North America. During the mid- produce only on certain tree species within 326 Havill · Foottit ANRV297-EN52-16 ARI 21 November 2006 10:26 Table 1 List of described adelgid species, their life cycles, secondary hosts, and native ranges Secondary Speciesa Life cyclec host genus Native range Reference(s) ◦ Adelges (Sacchiphantes) abietis (Linnaeus Anholocyclic 1 None Europe 28, 118, 126 1758) Adelges (Adelges) aenigmaticus Annand 1928 Unknown Larix Unknown 4 Adelges (Gilletteella) cooleyi (Gillette 1907) Holocyclic Pseudotsuga Western North 4, 30, 34, 67 America ◦ Adelges (Gilletteella) coweni (Gillette 1907) Anholocyclic 2 Pseudotsuga Western North 35, 127, 145 America Adelges (Sacchiphantes) diversis Annand 1928 Unknown Larix Unknown 4 ◦ Adelges (Adelges) geniculatus (Ratzeburg Anholocyclic 2 Larix Europe 145 1843) Adelges (Gilletteela) glandulae (Zhang 1980) Holocyclic Abies China 168 Adelges (Adelges) isedakii Eichhorn 1978 Holocyclic Larix Japan 54 ◦ Adelges (Adelges) japonicus (Monzen 1929) Anholocyclic 1 None Japan 54, 81, 113 ◦ Adelges (Dreyfusia) joshii (Schneider-Orelli Anholocyclic 2 Abies Western Himalayas 66 & Schneider 1959) Adelges (Sacchiphantes) karafutonis (Kono & Unknown Unknown Japan 54, 81 Inouye 1938) ◦ Adelges (Adelges) karamatsui Inouye 1945 Anholocyclic 2 Larix Japan 54, 81 Adelges (Sacchiphantes) kitamiensis (Inouye Unknown Larix Japan 82 1963) Adelges (Dreyfusia) knucheli Holocyclic Abies Western Himalayas 66, 91 (Schneider-Orelli & Schneider 1954) ◦ Adelges (Adelges) lapponicus (Cholodkovsky Anholocyclic 1 None Europe 28 1889) Adelges (Sacchiphantes) lariciatus (Patch Holocyclic Larix North America 4, 37, 117 1909) Adelges (Adelges) laricis (Vallot 1836) Holocyclic Larix Europe 23, 25, 33, 136, 168 Adelges (Dreyfusia) merkeri Eichhorn 1957 Holocyclic Abies Europe 43, 45, 49, 121 ◦ Adelges (Dreyfusia) nebrodensis (Binazzi & Anholocyclic 2 Abies Italy 13 Covassi 1991) Adelges (Dreyfusia) nordmannianae (Eckstein Holocyclic Abies Caucasus Mountains 51, 53, 97, 156 by Agriculture & Agri-Food Canada on 09/05/08. For personal use only. 1890) Adelges (Cholodkovskya) oregonensis Annand Unknown Larix Unknown 4 Annu. Rev. Entomol. 2007.52:325-349. Downloaded from arjournals.annualreviews.org 1928 Adelges (Aphrastasia) pectinatae Holocyclic Abies Europe, China, 54, 55, 81, 145 (Cholodkovsky 1888) Japan ◦ Adelges (Dreyfusia) piceae (Ratzeburg 1844) Anholocyclic 2 Abies Europe 14, 97, 156 ◦ Adelges (Dreyfusia) pindrowi Yaseen & Ghani Anholocyclic 2 Abies Western Himalayas 164 1971 Adelges (Dreyfusia) prelli (Grossmann 1935) Holocyclic Abies Caucasus Mountains 63, 64 ◦ Adelges (Sacchiphantes) roseigallis (Li & Tsai Anholocyclic 1 None China 93 1973) ◦ Adelges (Dreyfusia) schneideri Borner¨ 1932 Anholocyclic 2 Abies Caucasus Mountains 121, 145 (Continued ) www.annualreviews.org • Biology and Evolution of Adelgidae 327 ANRV297-EN52-16 ARI 21 November 2006 10:26 Table 1 (Continued ) Secondary Speciesa Life cyclec host genus Native range Reference(s) ◦ Adelges (Sacchiphantes) segregis Steffan 1961 Anholocyclic 2 Larix Europe 138 ◦ Adelges (Dreyfusia) tadomatsui (Inouye Anholocyclic 2 Abies Japan 54, 81 1945) Adelges (Adelges) tardoides (Cholodkovsky Holocyclic Larix Europe 23, 145 1911) ◦ Adelges (Adelges) tardus (Dreyfus 1888) Anholocyclic 1 None Europe 11, 145 Adelges (Sacchiphantes) torii (Eichhorn Holocyclic Larix Japan 54 1978) Adelges (Aphrastasia) tsugae Annand 1924 Holocyclic Tsuga China, Japan, 4, 76, 166 Western North America ◦ Adelges (Cholodkovskya) viridana Anholocyclic 2 Larix Europe 143 (Cholodkovsky 1896) Adelges (Sacchiphantes) viridis (Ratzeburg
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