B

dioecious holocycly r egg ovipara male gynopara egg alata (emigrant)

fundatrix male gynopara aptera alata

aptera alata anholocycly

FIGURE 1 Evolutionary development of generalized aphid life cycles. Initially, aphids developed monoecious holocycly (A) on an ancestral woody primary host, where aestivation occurred because sap amino acids were unavailable during summer growth cessation. Next, multiple subfamilies independently evolved dioecious holocycly (B), where viviparae moved to summer-growing herbaceous secondary hosts but returned to their ancestral host in autumn. In some aphids, secondarily monoecious holocycly (C) developed on the secondary host when the primary host was lost. Often in warm areas, where selection for an overwintering egg is not imposed, some populations of dioecious and secondarily monoecious holocyclic aphids may lapse into facultative anholocycly (D) on their secondary hosts; this condition may become obligate anholocycly if the ability to produce sexuals is lost.

viviparae allows very rapid buildup of numbers and collapse of generation time. When a viviparous nymph is born, it has the embryos of both its daughters and granddaughters within it, creating a "telescoping" of generations. Apterae have lost their wings and associated musculature to optimize reproduction. They produce more offspring per female than do alatae, which must invest resources in their flight apparatus. However, alatae produce progeny earlier in life than do apterae, giving their relatively reduced number of offspring a better generational turnaround time than apterae mothers can. Apterae are selectively produced when the host plant is a good source of nutrients. Once an aphid population has built, either inducing a crowding effect among apterae or stressing its host to the level of impacting nutrient levels, the population usually switches to produce alatae, which migrate to better situations. However, the risks of successful migration

FIGURE 2 Aptera (top) and alata (bottom) viviparae of M. persicae. Shown in split images with ventral (upper half) and dorsal (lower half) aspects with heads to the right. [Drawings by Tokuwo Kono, modified from Kono, T., and Papp, C. S. (1977). "Handbook of Agricultural Pests, Aphids, Thrips, Mites, Snails, and Slugs." California Department of Food and Agriculture, Sacramento.]

FIGURE 2 Aptera (top) and alata (bottom) viviparae of M. persicae. Shown in split images with ventral (upper half) and dorsal (lower half) aspects with heads to the right. [Drawings by Tokuwo Kono, modified from Kono, T., and Papp, C. S. (1977). "Handbook of Agricultural Pests, Aphids, Thrips, Mites, Snails, and Slugs." California Department of Food and Agriculture, Sacramento.]

are great, especially for monophagous aphids that feed on uncommon hosts, because the flight of alatae is wind-borne and relatively passive. Alatae can be blown over 1600 km, often across an ocean, and survive the trip. Upon successfully alighting on their proper host and feeding for a short time, alatae begin autolysis of their flight musculature, precluding further flight but self-cannibalistically providing nutrients for their offspring. The production of viviparae continues until fall conditions trigger production of the sexuals.

A second, more complicated dioecious life cycle (Fig. 1B) has independently evolved among several different aphid groups that show seasonal alternation between differing hosts. This dioecious cycle probably evolved in response to the seasonally inadequate supply of nitrogen-based nutrients, especially amino acids, on their primary host. The phloem sap that aphids feed on has limited nitrogen availability, and nitrogen is the limiting nutrient in aphid development. Woody deciduous plants normally translocate amino acids in quantity only during the spring, when they are foliating, and in the fall, when leaf senescence breaks down leaf protein and nitrogen is translocated to the roots for overwinter storage. Aphids groups evolving on and restricted to such plants face a nitrogen deficit during the summer, when active plant growth ceases and phloem sap is low or devoid of nitrogen. Such groups (e.g., Periphyllus spp.) may develop an aestivating nymph that halts growth until fall. Other aphid groups (e.g., Aphidinae) whose ancestors originated on deciduous woody plants, have evolved to leave those primary hosts during the late spring, after the nitrogen flush associated with foliation has ceased. In doing so, their spring alatae, as emigrants, migrate to herbaceous secondary hosts that actively grow and transport nitrogen during the summer. In the fall, however, as their secondary hosts die back, the aphids return to their woody primary host by producing migrating males and gynoparae. There, the aphid's sexuals, its males and oviparae, capture that host's fall nitrogen flush and mate to lay their overwintering eggs in anticipation of the spring nitrogen flush. Depending on the aphid or its group, the secondary hosts may vary from quite specific to a broad number of botanical groups; but the primary hosts are often specific to a plant genus. Most aphid lineages have adapted specific types of secondary hosts, such as grasses (e.g., Metopolophium dirhodum, rose-grain aphid), roots (e.g., Smynthurodes betae, bean root aphid), other woody plants (e.g., Hormaphis hamamelidus), or herbs (e.g., Macrosiphum rosae, rose aphid). Some aphids specialize on secondary hosts of a particular environmental ecotype; for example, Rhopalosiphum nymphae, waterlily aphid, uses aquatic plants in many plant families.

Some aphid lineages (e.g., Schizaphisgraminum, greenbug) have evolved beyond dioecious holocycly, entirely leaving their primary host to remain on their secondary host, in secondarily monoecious holocycly (Fig. 1C). However, an important form of year-round residence on the secondary host occurs in warmer climates, where populations do not require an egg for overwintering survival. Under such conditions, otherwise holocyclic dioecious or monoecious populations may lapse facultatively into anholocycly on their secondary hosts (Fig. 1D). If such populations remain anholocyclic long enough, they may eventually evolve into obligate anholocycly by losing the ability to produce sexual morphs, despite undergoing environmental conditions that normally trigger their production. Depending on the aphid lineage and its adaptation to its host(s) or their alternation, nearly all aphid morphs may be winged or wingless, but the morph's wing condition is specific to the aphid group.

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