Egg maturation strategy and its associated trade-offs: a synthesis focusing on Lepidoptera

Authors


*Mark A. Jervis, Cardiff School of Biosciences, Cardiff University, Cardiff CF10 3TL, Wales, U.K.

Abstract

Abstract.  1. Insects vary considerably between and within orders, and even within the same genus, in the degree to which the female's lifetime potential egg complement is mature when she emerges as an adult.

2. The ‘ovigeny index’ (OI) – the number of eggs females have ready to lay divided by the lifetime potential fecundity – quantifies variation in the degree of early life concentration of egg production, and also variation in initial reproductive effort.

3. Here, an integrated set of hypotheses is presented, based on a conceptual model of resource allocation and acquisition, concerning trade-offs at the interspecific level between initial investment in egg production (as measured by OI) and other life-history traits in holometabolous insects.

4. The evidence supporting each of these hypotheses is reviewed, and particular attention is paid to the Lepidoptera, as relevant life-history data are rapidly accumulating for this ecologically and economically important group.

5. There is evidence at the interspecific level supporting: (i) a link between OI and a trade-off between soma and non-soma in Trichoptera and Hymenoptera (the proportionate allocation to soma decreases with increasing OI); (ii) a negative correlation between OI and dependency on external nutrient inputs (via adult feeding) in Hymenoptera and in Lepidoptera; (iii) a negative correlation between OI and the degree of polyandry (and nuptial gift, i.e. spermatophore, use) in Lepidoptera; (iv) negative correlations between OI and resource re-allocation capabilities (egg and thoracic musculature resorption) in Hymenoptera and in Lepidoptera; (v) a negative correlation between lifespan and OI in Trichoptera, Hymenoptera, and Lepidoptera, indicating a cost of reproduction; (vi) a link between winglessness and an OI of one in Lepidoptera; (vii) a negative correlation between OI and the degree of female mobility in winged Lepidoptera; and (viii) a negative correlation between OI and larval diet breadth (as mediated by oviposition strategy) in Lepidoptera.

Introduction

Egg maturation strategy in insects

Most entomologists are aware that insects can differ markedly in the degree to which the female's lifetime potential egg complement is mature (ready for laying) at the time of adult emergence. Mayflies exemplify the case where all eggs are mature, and many mosquitoes represent the opposite extreme. It is not generally appreciated, however, that such variability also occurs within an insect order (e.g. Lepidoptera: Eidmann, 1931; Boggs, 1986, 1997a; Trichoptera: Stevens et al., 1999, 2000; Hymenoptera: Jervis et al., 2001, 2003; Diptera: Oldroyd, 1964), and even at lower levels within the taxonomic hierarchy (e.g. within a genus, as in the butterfly Euphydryas, Table 1). This variation in initial investment in reproduction has adaptive significance, affecting not only short-term fitness (via female age-specific realised fecundity) but also lifetime reproductive success (Flanders, 1950; Boggs, 1986; Rosenheim, 1996; Heimpel & Rosenheim, 1998; Heimpel et al., 1998; Rosenheim, 1999a, b; Ellers et al., 2000; Papaj, 2000; Roitberg, 2000; Rosenheim et al., 2000; Jervis et al., 2001; Ellers & Jervis, 2003, 2004).

Table 1.  Lepidoptera for which an OI value is known (based on dissections of newly emerged females) or (e.g. in the case of Saturniidae) has been surmised based on oviposition data. Lifespan data (days) are mean values (measured under laboratory conditions), unless otherwise stated; the statistical analysis undertaken by M. A. Jervis, C. L. Boggs and P. N. Ferns (unpublished data, see text) used data only from those species for which laboratory means were available. Known feeding habits: Ne, nectar-feeder; Po, pollen-feeder; Ho, honeydew-feeder; Su, feeds on sugar-rich fluids; Mu, mud-puddler; Ca, feeds on carrion fluids; Fe, feeds on faecal fluids; Fr, feeds on fluids contained in rotting fruit (note that Mu, Ca, Fe, and Fr are frequently linked); NF, non-feeding. Flight mobility/dispersal: sedentary species are defined as typically dispersing the order of only 10s to 100s of metres or less during their lifetimes; semi-vagile is defined as having a more open population structure; vagile is defined as exhibiting migratory behaviour or seasonal range expansion [a classification scheme taken from Wilcox et al. (1986) and Boggs and Murphy (1997)]. The aforementioned categorisation does not take account of sex differences, but note that, at least in moths, females are sedentary compared with males. Eggs: ‘clusters’ includes laying of eggs in elongate masses.
 OvigenyLifespanFeedingMatingResorptionFlight mobility/Eggs: laid singly 
Lepidopteraindex(days)habitsystemcapabilitydispersalor as clustersSource
MONOTRYSIA
HEPIALOIDEA
Hepialidae (generally)1 or ≈ 1
(at least
some
species)
 NF  Macropterous,
females sedentary
SinglyMiller (1996),
G. Tordoff
(pers. comm.)
DITRYSIA
YPONOMEUTOIDEA
Yponomeutidae
Plutella xylostella (L.)0–0.0418.8Ne  Macropterous,
vagile
SinglyPivnick et al.
(1990), Yusoh
(1999)
, D. J. Wright
(pers. comm.)
GELECHOIDEA
Gelechiidae
Pthorimaea operculella
(Zeller)
0.13522 max.Ne, Su  MacropterousSingly or
clusters
Graf (1917),
Fenemore (1977)
SESIOIDEA
Sesiidae
Synanthedon pictipes
(Grote & Robinson)
<0.59.2   MacropterousSinglyGreenfield &
Karandinos (1976)
TORTRICOIDEA
Tortricidae
Zeiraphera canadensis
Mutuura & Freeman
0.3621.6   MacropterousClustersCarroll & Quiring
(1993),
Ostaff & Quiring
(1994)
PYRALOIDEA
Pyralidae
Cadra cautella (Walker)010.6Probably Su in the wild,
but there is evidence that
feeding does not affect
realised fecundity.
  Macropterous,
females sedentary
 Norris (1934)
Ephestia kuhniella Zeller<<111.6As for C. cautella  Macropterous,
females sedentary
 Norris (1932, 1934)
Margaritia sticticalis (L.)<<1 Ne  Macropterous Norris (1934)
Ostrinia nubilalis
(Hübner)
013SuPolyandry MacropterousClustersLeahy & Andow
(1994),
Fadamiro & Baker
(1999),
Xingquan et al.
(2004)
Pleuroptya ruralis (Scopoli)037Ne  Macropterous,
females sedentary
 Romanowski (1991)
Plodia interpunctella
(Hübner)
0 or ≈ 06–17SuPolyandry Macropterous,
females sedentary
Singly or
clusters
Norris (1932),
Gage (1995, 1998
),
Huang &
Subramanyam (2003)
BOMBYCOIDEA
Bombycidae (generally)1Very short- lived
(a few days)
NF    Eidmann (1931)
Sphingidae<1 and
apparently >0
Generally long-lived,
but Janzen
(1984)
mentions a
tropical species
that lays all of
its eggs in 1 week
Ne (long-tongued spp.),
NF (short-tongued spp.);
homeothermic,
i.e. high carbohydrate
requirement
  Macropterous,
typically heavy-bodied,
strong fliers, semi-vagile,
some species vagile
SinglyMell (1922, 1940),
Janzen (1984), Miller
(1997)
Saturniidae (generally)1Some very short-
lived [e.g.
Hyalophora cecropia
L. and H. gloveri
(Srecker)], others
longer-lived, e.g.
Callosamia
promethea
(Drury)
(max. 10)
Mostly non-feeders despite
being homeothermic
  MacropterousTypically clustersRau & Rau (1913),
Miller (1978), Miller
& Cooper (1977),
Gardiner (1982),
Janzen (1984),
Saito (1992)
Heinrich (1993),
Miller (1996)
LASIOCAMPOIDEA
Lasiocampidae (generally)1 (most, if not
all species)
Short-livedNF [include
Lasiocampa
quercus
(L.)
and Malacosoma
neustria
(L.)]
  MacropterousEither singly
(L. quercus) or clusters
(M. neustria)
Scoble (1995),
G. Tordoff
(pers. comm.)
NOCTUOIDEA
Noctuidae
Diparopsis castanea Hampson0.6110.8 (single-mated) Polyandry Macropterous, vagile Marks (1976)
Euxoa messoria (Harris)014.2Feeder?
[E. nigricans L. and
Eobelisca
(D. & S.) feed]
  MacropterousSinglyCheng (1972),
Miller (1996)
Heliothis virescens (F.)011.3Su, Ne  Macropterous, vagileSinglyProshold et al. (1982),
Willers et al. (1987),
Peck et al. (1999)
Panolis flammea (Denis &
Schiffermüller)
≈ 0.214 (field), max.
24 (lab.)
Ne  MacropterousSingly and clustersLeather (1984),
Leather & Bernand (1987)
,
S. R. Leather (pers.
comm.)
Spodoptera exempta (Walker)08.1Ne, Ho  Macropterous, vagileClustersGunn & Gatehouse
(1965)
Spodoptera exigua (Hübner)<<1‘10–16’SuPolyandry Macropterous, vagileClustersTisdale & Sappington
(2001),
Torres-Vila et al.
(2001), Showler &
Moran (2003)
Spodoptera litura (Fab.)0    Macropterous, vagile,
migratory
 Murata & Tojo
(2002)
Lymantriidae (generally)1 or >>0Some species very
short-lived, others
longer-lived
NF [including
Euproctis
chrysorrhea
(L.),
Euproctis similis
(Fuessly),
Lymantria dispar,
O. antiqua]
  Some macropterous,
others apterous;
macropterous species
mainly weak fliers.
 Eidmann (1931),
Barbosa et al. (1989),
Miller (1996)
Lymantria dispar (L.)1 or <110.5NF  Macropterous,
N. American
populations
highly sedentary,
Asian ones significantly
less so
ClustersNorris (1934),
Barbosa et al. (1989),
Miller (1996),
Proshold (1996)
,
Elkinton & Liebhold
(1990)

R. J. C. Cannon
(pers. comm.)
Lymantria monacha (L.)1≈ 10NFMonandry Macropterous,
semi-vagile
 M. Keena (pers.
comm.)
Bejer (1988)
Orgyia antiqua (L.)1≈ 7NF  Apterous, females
sedentary
ClustersTammaru et al. (2002),
G. Tordoff
(unpublished)
GEOMETROIDEA
Geometridae
Biston betularia (L.)14.4NF  Macropterous,
semi-vagile
ClustersBishop (1972), Miller
(1996)
, D.R. Lees
(pers. comm.)
Bupalus pinarius (L.)<19.9NF  Macropterous,
semi-vagile
Singly and clustersŠmits et al. (2001),
S. R. Leather
(pers. comm.)
Erranis defoliaria (Clerck)1<<7NF  Brachypterous
(flightless),
females highly
sedentary
ClustersMiller (1996),
D. R. Lees
(pers. comm.)
Operophtera brumata (L.)1<<7NF  Brachypterous
(flightless),
females highly
sedentary
ClustersMiller (1996),
D. R. Lees
(pers. comm.)
PAPILIONOIDEA
Papilionidae
Battus philenor (L.)0 NePolyandry Macropterous,
semi-vagile
ClustersOdendaal (1989),
Odendaal &
Rauscher (1990)
Battus polydamas (L.)0>35Ne  Macropterous,
semi-vagile?
 Young (1972)
Papilio anchisiades Esper0>35Ne  Macropterous,
semi-vagile?
 Young (1972)
Papilio xuthus L.0.004 Ne Resorbs eggsMacropterous,
semi-vagile?
 Watanabe (1988)
Parides childrenae (Gray)0>35Ne  Macropterous Young (1972)
Parides eurimedes (Stoll)0>30Ne  Macropterous Young (1972)
Pieridae
Colias erate (Esper)0 NePolyandry Macropterous Nakanishi et al.
(2000)
Colias eurytheme Boisduval024Ne, MuPolyandry Macropterous,
semi-vagile
SinglyStern & Smith (1960),
O'Brien et al. (2004),
Kemp & Rutowski
(2004)
Pieris brassicae (L.)036 max.NePolyandry Macropterous, vagileClustersFeltwell (1982)
Pieris napi (L.)024 max.Ne, MuPolyandry Macropterous,
semi-vagile
SinglySculley & Boggs
(1996),
Wiklund et al. (2001)
,
F. Chew et al.,
unpublished
Pieris rapae (L.)<<113NePolyandry Macropterous,
semi-vagile
SinglyRichards (1940),
Jones et al. (1980),
Sutcliffe et al. (1996),
Wiklund et al. (2001)
Lycaenidae
Jalmenus avagoras (Donvan)<<123.5Ne  Macropterous Hill & Pierce (1989)
Nymphalidae
Anartia fatima Godart‘some’
(few relative to
lifetime
fecundity)
>15Ne  MacropterousSinglyYoung (1972),
Feldman & Haber
(1998)
Brassolis sophorae (L.)<19NF  Macropterous,
semi-vagile
 Carvalho et al. (1998)
Danaus plexippus (L.)025.5 (non-
migratory adults;
migratory adults
live for several
months in field)
NePolyandry Macropterous,
semi-vagile
to vagile,
depending on
population
SinglySvard and Wiklund,
1988, Oberhauser (1997),
Herman & Tatar (2001),
Meitner et al. (2004)
Dryas iulia (Fab.)022.4NePolyandry Macropterous, vagileSinglyDunlap-Pianka et al.
(1977), Boggs (1979)
Euphydryas editha
(Boisduval)
0.174–0.178, varies
with locality
12Ne, MuPolyandry Macropterous,
females
sedentary
ClustersLabine (1964, 1968),
Murphy et al. (1983),
Launer et al. (1993),
Boggs (1997a,
b), Boggs
& Nieminen (2004),
Hellmann et al. (2004)
Euphydryas chalcedona
(Doubleday)
0.04515NePolyandry Macropterous,
females
sedentary
ClustersBrown & Ehrlich (1980),
Rutowski &
Gilchrist (1987),
O'Brien et al. (2004)
Heliconius charitonia (L.)037.4, with a
maximum of
>4 months in field
Ne, PoMonandryResorbs eggsMacropterous,
vagile
SinglyDunlap-Pianka et al.
(1977), Boggs (1979),
Waller & Gilbert (1982),
Quintero (1988),
Boggs (1990),
O'Brien et al. (2003)
Heliconius cydno Doubleday044.4Ne, PoPolyandry Macropterous,
semi-vagile
SinglyBoggs (1979)
Heliconius hecale (Fab.)0Similar to H. cydnoNe, PoPolyandry Macropterous,
semi-vagile
SinglyDunlap-Pianka et al.
(1977), Karlsson (1994),
Penz & Krenn (2000)
,
C. L. Boggs,
unpublished
Mycalesis perseus (Fab.)018 max.FrPolyandry Macropterous,
vagile
SinglyBraby (1995, 2002),
Braby & Jones (1995)

M. F. Braby (pers.
comm.)
Mycalesis sirius (Fab.)017.15Ne (rarely)Polyandry Macropterous,
vagile
SinglyBraby (1995, 2002),
Braby & Jones (1995)
,
M. F. Braby (pers.
comm.)
Mycalesis terminus (Fab.)021.62FrPolyandry Macropterous,
vagile
SinglyBraby (1995, 2002),
Braby & Jones (1995)
,
M. F. Braby (pers.
comm.)
Siproeta (Victoriana)
stelenes
(L.)
0>40Ne  Macropterous Young (1972)
Speyeria idalia (Drury)0>8 weeks in field.
Females undergo
reproductive diapause;
mature eggs
are not produced
until late in life
NeMonandry Macropterous Kopper et al. (2001)
Speyeria mormonia Edwards021.2Ne, Mu, Fe, CaMonandryResorbs eggsMacropterous,
semi-vagile
SinglyBoggs (1986),
Boggs (1987),
Boggs & Jackson (1991),
Boggs & Ross (1993),
Karlsson (1994),
Sculley & Boggs (1996),
O'Brien et al. (2004)

The overall degree of egg maturation achieved by newly emerged females is correlated with a number of other adult life-history traits involved in resource allocation and acquisition: (1) allocation-related traits: (a) lifespan (Flanders, 1950; Boggs, 1986, 1997a; Ellers & van Alphen, 1997; Jervis et al., 2001, 2003), (b) egg type (the degree of yolk-poorness, linked to the need, by the eggs of some parasitoids, to absorb host fluids) (Jervis et al., 2001), (c) allocation of abdominal resources to storage (fat body) vs. eggs (Ellers & Jervis, 2003, 2004), (d) egg resorption capability (Jervis et al., 2001), (e) the role of nuptial gifts in female reproduction (Boggs, 1990), and (f) body size (Ellers & Jervis, 2003, 2004; Jervis et al., 2003; Jervis & Ferns, 2004); (2) acquisition-related traits: (g) mouthpart structure (Eidmann, 1931; Miller, 1997; Gilbert & Jervis, 1998; Jervis, 1998), (h) adult feeding habit (Eidmann, 1931; Flanders, 1950; Boggs, 1986; Jervis & Kidd, 1986; Jervis et al., 1993; Miller, 1996; Gilbert & Jervis, 1998; O'Brien et al., 2004), (i) the degree of host fidelity (in parasitoids: Roitberg, 2000), and (j) the proportion of attacked hosts used by the parasitoid female for her own feeding purposes (Jervis & Kidd, 1986).

The available empirical data and/or theoretical modelling outputs link traits (a), (c), (f), (i), and (j) with egg maturation strategy at the intraspecific level, and traits (a), (b), and (d)–(h) at the interspecific level. This array of correlations – positive in some cases, negative in others – suggests the existence of adaptive suites of life history traits involving trade-offs based on allocation patterns. Examination of whole suites, rather than the traditional approach of focusing on just a pair of traits, can facilitate understanding both of the diversity and of the evolution of insect life histories, as has been advocated by Boggs (1986, 1990, 1997a), Blackburn (1991a, b), Gilbert and Jervis (1998); Mayhew and Blackburn (1999), Jervis and Vilhelmsen (2000), Jervis et al. (2001), and O'Brien et al. (2004).

Here, a previously developed measure of initial investment in reproduction is explained. Next, an integrated set of hypotheses regarding trade-offs between early life investment in egg production and other traits is outlined. Then, the review considers evidence for these hypotheses, taken from among Trichoptera, Hymenoptera, Diptera, and Lepidoptera (data relating to Coleoptera could not be found). It concentrates on Lepidoptera because relevant life-history data are rapidly accumulating for these insects with respect to the aforementioned hypotheses.

The ovigeny index

The proportion of a female's eggs that are mature and ready to lay at adult emergence is measured by the ‘ovigeny index’ (OI) – the ratio (expressed as a proportion) of the initial egg load (fully mature eggs) to the lifetime potential fecundity (Jervis et al., 2001). An OI of one signifies that all the oocytes are mature upon emergence, whereas an OI of zero signifies emergence with no oöcytes ready to lay. OI varies from zero to one among Hymenoptera (Jervis et al., 2001) and also among Lepidoptera (Table 1). There is an obvious continuum of OI among Hymenoptera (Jervis et al., 2001) and there appears to be a continuum also among Lepidoptera (Table 1).

OI measures both the degree of early life concentration of lifetime egg production within the female adult, and the relative allocation of resources to reproduction, by the juvenile and the adult stages (Jervis et al., 2001; Jervis & Ferns, 2004). If OI is close to one, larval resources are the sole or nearly sole sources for egg maturation, corresponding to the concept of ‘capital’ breeding (e.g. Sibly & Calow, 1984, 1986; Boggs, 1992, 1997a; Stearns, 1992; Tammaru & Haukioja, 1996; Jönsson, 1997; Bonnet et al., 1998). In contrast, if OI is close to zero, larval resources (e.g. from fat body) likely account for at most a small proportion of the resources that are allocated to oögenesis, with adult foods or male nuptial gifts being the most likely other sources, although in some species nutrients required for later-life egg production, but missing from the adult diet, must derive from larval feeding (e.g. Boggs, 1981, 1986, 1994, 1997b; Rivero et al., 2001; O'Brien et al., 2002; O'Brien et al., in press). This scenario, when OI is close to zero, corresponds to the concept of ‘income’ breeding.

In spite of its advantages, OI does not perfectly measure the absolute amount of resources invested in reproduction at adult emergence. If OI is not one, immature oöcytes may be partially yolked prior to adult emergence (e.g. 4–7% of total volume in some Lepidoptera, O'Brien et al., 2004; see also Jervis & Ferns, 2004). Also, nurse cells (trophocytes) that are associated with the immature oocytes can contain non-trivial amounts of resources (Jervis & Ferns, 2004). Nevertheless, within or among insect species possessing equivalent ovarian developmental systems, OI can be assumed to correlate with pre-emergence reproductive effort, at least when the latter is measured as the proportion of the adult's biomass that is invested in offspring (see Jervis & Ferns, 2004 for a review of the evidence). Thus, here, OI is used as an unbiased estimator when making interspecific comparisons within insect orders such as the Lepidoptera, the Hymenoptera, and the Trichoptera, although we caution against using OI for making comparisons between taxa possessing different ovarian developmental systems.

A conceptual model of resource allocation and acquisition

It is assumed that the degree of resource investment in eggs at adult emergence, measured by OI, is the result of underlying functional trade-offs among physiological traits, dependent both on resource acquisition and on allocation during the entire life of the insect. Thus, resource acquisition and allocation, together with ideas relating to investment of capital and income, can be used to organise an array of hypotheses concerning suites of OI and other key life-history traits. It must be stressed, however, that allocation to reproduction prior to adult emergence (OI), although chosen as the key element around which to organise this review, may not necessarily have driven the evolution of the suites of traits, i.e. it may not be the case that it ‘organises’ life-histories [cf. larval development mode in parasitoid wasps (Mayhew & Blackburn, 1999)].

The overall conceptual framework first connects OI to broad resource allocation and acquisition patterns. As OI is a measure of the degree of initial, direct capital investment in reproduction, it is expected to reflect trade-offs between other initial allocations (Fig. 1). Also, as a measure of initial capital investment, OI can be expected to be inversely related to anticipated investment of income in reproduction. Finally, it is expected that OI will be inversely related to the ability to re-allocate resources once they are committed to eggs or soma. Building on these allocation patterns, it is then postulated that correlations exist between OI and a range of key life-history traits in females: lifespan, feeding habit, mobility, and oviposition strategy. The net result is a hypothesised set of integrated suites of life-history and allocation/acquisition traits (Table 2). Thus allocation patterns, along with life-histories and aspects of individual behavioural ecology (all of which potentially affect population structure and dynamics, see Kidd & Jervis, 1989; Miller, 1996; Tammaru & Haukioja, 1996; Jervis & Kidd, 1999; Boggs, 2003) are tied together. Several of the hypotheses have some support from one or another insect order, generally the Lepidoptera and Hymenoptera, but evidence from the orders Trichoptera and Diptera is also presented.

Figure 1.

Allocation of carried-over (capital) resources to competing physiological functions within adult female holometabolous insects.

Table 2.  Predicted variation in different life-history traits in relation to variation in OI. Trait states specified are tendency or likelihood, except in the case of lifespan, host-plant range and clutch size. Evidence in support of each hypothesis is discussed in the text. The predicted variation in lifespan has been confirmed by M. A. Jervis, C. L. Boggs and P. N. Ferns (unpublished data), using methods (which control for phylogeny).
 Low OIIntermediate OIHigh OI
Life-history variable(0 or ≈ 0)(<<1, >>0)(1 or ≈ 1)
Allocation to initial reproductive effortLowIntermediateHigh
Allocation to soma vs. non-somaHighIntermediateLow
Proportional allocation of non-soma to reserves vs. initial eggsLowHighLow
Dependency on exogenous nutrients (adult foods, nuptial gifts)HighIntermediateLow
Resource re-allocation capability (eggs and/or muscle resorption)Often presentRarely presentAbsent
LifespanLowIntermediateLow
Wing reductionLowLowHigh
Female flight mobilityHighIntermediateLow
Larval host plant rangeNarrowIntermediateBroad
Egg depositionSingle eggSingle and/or clustersClusters

The aforementioned suites of life-history traits are expected ‘all else being equal’. There are, however, competing hypotheses concerning the underlying mechanisms of negative correlations between life-history traits (e.g. see Weinert & Timiras, 2003 for a review with respect to ageing theory). In particular, the resource limitation basis of negative correlations involving reproduction has recently been called into question by findings from the nematode Caenorhabditis elegans (Maupas), which suggest that the signalling pathway controlling reproduction and lifespan operates on the two functions independently (reviewed by Barnes & Partridge, 2003). However, as Barnes and Partridge (2003) argue, the implication for resource allocation as a major determinant in the evolution of trade-offs is not yet clear. The approach here is to assume that trade-offs have evolved in the context of a given range of resource availability, there being at least some degree of resource limitation, even though the latter may not be the ultimate cause of the observed patterns.

Interaction of initial reproductive investment with other allocation patterns

Trade-offs with other initial allocations

Given that OI is an estimator of initial (i.e. pre-adult) reproductive effort, and hence of initial capital investment, it is expected to be linked to the following trade-offs: between reproduction and soma, and between eggs and other non-soma (Fig. 1, Table 2) (soma comprises body structures other than internal reproductive tissues, oöcytes, and nutrient stores, e.g. fat body):

1. The trade-off between reproduction and soma.  Generally in holometabolous insects, most of the investment in soma has occurred by the time of adult emergence. Thus, soma and reproduction are likely to compete, during late ontogeny, for initial adult resource allocation (Fig. 1), resulting in a trade-off between soma and OI. This is an extension of Boggs' (1981) hypothesis, which did not consider OI. That hypothesis predicts that, all else being equal, holometabolous species whose females are longer-lived and which have higher resource intake prospects should invest more in building a ‘sturdy body’ (soma) at the expense of non-soma. Empirical support for Boggs' hypothesis was provided by her comparative study of three heliconiine butterfly species with differing lifespans and adult feeding habits (Boggs, 1981); however, OI = 0 for all these species. Some support for a trade-off between OI per se and soma is provided by Stevens et al. (1999, 2000) in their study of Trichoptera. In the two caddis fly species examined, Glyphotaelius pellucidus (Retzius) has an OI approaching zero, and its (dry mass) investment in thorax vs. total body is 45%, whereas Odontocerum albicorne (Scopoli) has an OI approaching one, and its investment is 33% (D. J. Stevens, unpublished data). Additionally, body size per se can be used as a crude measure of allocation to soma. In this case, a cross-species negative correlation between OI and body size is expected, as occurs among Hymenoptera (Jervis et al., 2003), a relationship explained mainly by variation in initial egg load (the numerator in the OI) (Jervis & Ferns, 2004). However, in Lepidoptera body size can theoretically influence OI also through its effect on lifetime potential fecundity (the denominator in the OI) (see García-Barros, 2000).

2. The trade-off between eggs and reserves within non-soma.  At female emergence, non-soma is partitioned among initial eggs and reserves, the latter having the potential for use in either reproduction (future eggs) or survival (upon which future egg production and deposition depend) (Wheeler, 1996) (Fig. 1).

There is currently a lack of precise data relating to allocation within non-soma and its implications for the fuelling of somatic maintenance, at the interspecific level. However, the results of Herz and Heitland, 2002 study of fat allocation among five ‘strictly pro-ovigenic’ (sensuJervis et al., 2001; OI = 1) diprionid sawfly species point to an initial egg load vs. reserves trade-off. Two species allocated most of their total body fat to initial eggs, one species allocated most of its fat to other tissues (in most holometabolous insects, the fat body constitutes the principal store of lipids, Chapman, 1998), and two species allocated the fat evenly. It is reasonable to infer that if such variation in allocation between eggs and reserves can occur among species having the same OI, it can similarly occur among species having different OIs [there is support for this inference from the study by Ellers & van Alphen (1997) of resource allocation in clinal populations of the parasitoid wasp Asobara tabida (Nees), discussed below]. If so, how would allocation of non-soma to eggs vs. reserves vary with OI among species? Interspecifically, the proportionate allocation to reserves should generally be least for species with an OI of either zero or one, and greatest for species with an intermediate OI. At OI = 0, expected income is high (see below), reducing the requirement for reserves. Migratory Danaus plexippus (OI = 0) do indeed have a small quantity of reserves at emergence: the fat body comprises less than one-fifth of the total body weight, compared with later on in life in this long-lived species (>40%) (Brower, 1985) (Table 1). With OI = 1, egg maturation is complete, so reducing the requirement for reserves, and expected lifespan is low (see below), consequently reducing the amount of time available to use them. Predicted allocation between eggs (OI) and reserves thus incorporates an expected reproduction – survival trade-off. These predictions are for reserves as a biochemical whole. Given that the diets of larvae and adults may vary in biochemical composition, particular storage compounds may vary in different ways (see Wheeler et al., 2000; for an investigation in which specific materials were individually measured).

Exceptions to the above predictions are expected to occur, and there is indeed evidence to this effect. A cyclorraphan dipteran with an OI = 0, and also some diprionid sawflies (OI = 1, see above) emerge with non-trivial amounts of lipid reserves (Spradbery & Sands, 1981; Herz & Heitland, 2002 respectively), and specimens of Lasiocampidae (OI = 1 in most species, Table 1) are renowned among lepidopterists for becoming visibly greasy, post-mortem (Leverton, 2001). A priori, low-OI species in environments with variable adult food availability are likely to be under strong selection to evolve a risk-averse strategy involving increased allocation to reserves (see Jervis et al., 2001; Boggs, 2003). Alternatively, species whose females cannot obtain key nutrients for oögenesis from their adult diet will need to carry-over sufficient quantities of these from the larval stage (see above). Species that undergo adult reproductive diapause (each of the orders Lepidoptera, Hymenoptera, Trichoptera, and Diptera includes examples, see Oldroyd, 1964; Cole, 1967; Spradbery, 1973; Stevens et al., 2000; Herman & Tatar, 2001; Kopper et al., 2001; Majerus, 2002) also would be expected to show relatively high allocation to reserves and thus a low OI at adult emergence, although migratory monarch butterflies clearly do not conform to this pattern (see above). With regard to high-OI species, it would seem likely that, in environments in which variability in oviposition opportunities results in a significant degree of time limitation, there will be selection for a risk-aversion strategy involving increased allocation to reserves, allowing lifespan to be sufficiently extended for the remainder of the mature egg complement to be laid. Although this hypothesis is at variance with the results of theoretical modelling conducted on parasitoid wasps (Ellers et al., 2000), it might apply to some other holometabolous insects.

Empirical evidence for a potential interspecific relationship, linking OI with relative allocation to eggs and reserves, is provided by a parasitoid wasp (Hymenoptera), Asobara tabida. This species shows north – south clinal variation within western Europe: the southern and northern populations differ with respect to OI, southern females having the higher OI (but same lifetime realised fecundity), the lower allocation to body fat, and the shorter life span (Ellers & van Alphen, 1997). It is tempting to conclude that these differences are the result of natural selection, adapting populations to local conditions (northern and southern populations experience different levels of host availibility, Ellers & van Alphen, 1997), and that interspecific differences in OI and partitioning of reserves might arise similarly.

Interaction with resource income

‘Resource income’ refers to external nutrient inputs to the adult stage. In holometabolous insects, these can include nutrients from adult food (Gilbert & Jervis, 1998) and, in some cases, male nuptial donations to the female (Boggs & Gilbert, 1979; reviewed in Boggs, 1995). In general, it is expected that OI should be inversely correlated with availability and nutritional completeness of resource income, whether from food or from nuptial gifts. This again parallels ideas relating to the role of larval vs. adult resources in reproduction developed in Boggs (1981, 1990, 1997a), but here explicitly considers the interaction of initial capital expenditures, in the form of OI, with resource income.

1. OI and dependency on adult feeding.  Empirical support for a negative relationship between these two variables is available from Hymenoptera (see Jervis & Kidd, 1986; Jervis et al., 2001). As another example, among Lepidoptera, the available evidence suggests that low quality or quantity of adult food, along with low nutrient input from spermatophores (male nuptial gifts), is linked to a higher OI (Eidmann, 1931; Norris, 1934, 1936; Boggs, 1986, 1997a; O'Brien et al., 2004) (Table 1). Additionally, lepidopteran species not feeding as adults typically have an OI = 1 (Common, 1990), except for Lymantria dispar (L.) (Lymantriidae), in some circumstances, Bupalus piniarius (L.) (Geometridae) and Brassolis sophorae (L.) (Nymphalidae), for which OI is high but not one (Table 1). By contrast, all the species in Table 1 that are known to be feeders have an OI < 1 (OI = 0 in the majority of cases). Heliconius species, which feed not only on nectar but also on the contents of pollen grains (Gilbert, 1972; Penz & Krenn, 2000), have an OI = 0 (Dunlap-Pianka et al., 1977; Boggs, 1990; O'Brien et al., 2003), while feeders on other nitrogen-rich materials such as fluids from faeces and cadavers, likewise have an OI = 0 (Table 1).

2. OI and monandry/polyandry (nuptial gifts).  The amount of nutrient acquisition in the form of nuptial gifts will be higher for polyandrous species than for monandrous species, and will increase with the degree of polyandry if spermatophores are of equivalent relative size and absorbability (Boggs, 1990; also see Karlsson, 1994, 1995, 1998). Thus, OI and mating frequency are predicted to be negatively correlated. There are insufficient data to test this hypothesis, but note that, in accordance with the hypothesis, all of those species in Table 1 identified as being polyandrous have an OI << 1.

Interaction with the ability to re-allocate initial capital resources

Based on relationships between OI, lifespan, income resources, and allocation to soma and to reserves outlined above, OI is expected to be inversely related to the ability to re-allocate capital resources such as egg materials or thoracic musculature during adult life. Egg resorption capability ought to be most common among low-OI species, because resorption takes several hours to days, and if concurrent in all ovaries, precludes oviposition (Jervis & Kidd, 1986). Thus, resorption ought to be least costly, in terms of the female's time budget, for longer-lived species. Similarly, thoracic muscle resorption is a relatively slow process, so it is unlikely to occur in short-lived species (i.e. OI = 1 or ≈ 1), which have little need for additional nutrients for egg production.

Parasitoid wasps show a strong inverse relationship, across species, between OI and egg resorption capability (Jervis et al., 2001). Some Hymenoptera also resorb thoracic musculature, e.g. the parasitoid wasp Pimpla turionellae, which has an OI = 0 (Sandlan, 1979). There are insufficient data to test the hypothesis in Lepidoptera, but note that among the species in Table 1 egg resorption capability is confined to species with an OI = 0 or ≈ 0, in accordance with the prediction. Additionally, Stjernholm and Karlsson (2000) showed that nutrients released from the thorax contribute to egg production in one lepidopteran species, and Stjernholm et al. (in press) document changes in thoracic mass with age in a number of species. This suggests that the possibility exists for a relationship with OI.

Note that egg resorption and thoracic musculature resorption capabilities are not necessarily mutually exclusive. Pimpla turionellae practises both types of re-allocation when deprived of hosts: muscle resorption is employed first, allowing egg production to continue until egg resorption is used as a ‘last resort’ survival tactic (Sandlan, 1979; see also Jervis & Kidd, 1986 for a review). In this species the degree of muscle resorption depends on whether females have access to external nutrient inputs (Sandlan, 1979). In contrast, in butterflies the use of thoracic nutrients occurs particularly when females are able to feed and have received nuptial gifts, apparently in response to extrinsic nutrient intake, and it commences in some species at a relatively early age, proceeding more or less steadily thereafter (Karlsson, 1998; Stjernholm & Karlsson, 2000; Stjernholm et al., in press).

Interaction of initial reproductive investment with life-history traits

Trade-off with adult lifespan

In general, life-history theory based on resource allocation predicts an inverse correlation between reproductive effort and life expectancy, as a cost of reproduction (e.g. Bell & Koufopanou, 1986; Barnes & Partridge, 2003; Weinert & Timiras, 2003). Given that OI is a measure of initial investment in reproduction, adult lifespan is therefore expected to decrease with increasing OI.

At the interspecific level, lifespan and the degree of egg maturation at adult emergence are indeed negatively related, in a phylogenetically diverse array of Lepidoptera (M. A. Jervis, C. L. Boggs and P. N. Ferns, unpublished data). Among parasitoid wasps OI and adult lifespan are negatively correlated both within (Jervis et al., 2001; using data in Ellers & van Alphen, 1997) and between species (Jervis et al., 2001; Jervis et al., 2003). OI and lifespan appear also to be negatively correlated among caddis flies (Trichoptera) [based on data in Novak & Sehnal (1963) and unpublished data sets of D. J. Stevens and J. Jannot].

Trade-off with female mobility

Previous workers on Lepidoptera have reasoned that a large initial egg load (which results from a high OI combined with a high lifetime potential fecundity) should tend to preclude much pre-oviposition dispersal (Labine, 1968; Chew & Robbins, 1984), in accordance with the oogenesis – flight syndrome theory of Johnson (1969). This phenomenon could occur via increased wing loading due to increased abdominal mass (Labine, 1968; Chew & Robbins, 1984; Sattler, 1991; but see Kingsolver, 1999; Marden, 2000) and/or competition between the ovarian tissues and the thoracic musculature for limited body space (Tweedie, 1976; Kaitala, 1988; Sattler, 1991; but see Stjernholm et al., in press). Additionally, as a recent investigation by Hanski et al. (2004) demonstrates, changes in metabolic rate could play a role in altering intraspecific dispersal tendency in Lepidoptera; in that study, differences in dispersal tendency were also associated with effects on potential fecundity in large females, but the effect of metabolic changes associated with dispersal on OI is unknown.

Available data to test the predicted trade-off between OI and female mobility mainly relate to Lepidoptera, and are of two forms. First, in the extreme, female winglessness (aptery) is associated with reduced feeding capability and a high degree of egg maturation in emergent females (high OI) (Sattler, 1991). Second, data are accumulating that suggest a negative correlation between OI and the degree of female mobility in winged species (Table 1).

Nonetheless, the relationship in respect of wing reduction – high OI might be ‘noisy’: the families Bombycidae, Saturniidae, and Lasiocampidae, despite being characterised by an OI = 1, do not contain taxa that have opted for either brachyptery or aptery (some members of the Lymantriidae have, however, done so) (Table 1). The same caution applies to the hypothesis in respect of mobility of winged Lepidoptera, as some of the very low-OI species in Table 1 are sedentary, but note that in accordance with the hypothesis, all of the migratory species have an OI << 1.

Interaction with oviposition strategy

A female's oviposition strategy has several components, which include the range of substrates oviposited on (host plant species, in the case of insect herbivore groups such as Lepidoptera), and also clutch size. It is postulated here that in Lepidoptera these two behavioural traits are tied to OI, via constraints relating to oviposition opportunities and the time available for dispersal.

All else being equal, females of polyphagous species should experience a greater likelihood of locating suitable oviposition sites, so can be expected to have high initial egg availability (high OI) [at least among parasitoid Hymenoptera, initial egg load and OI are very strongly correlated, Jervis & Ferns (2004)]. Females of species with narrower host ranges, by contrast, may run a greater risk of not locating sufficient oviposition sites, so can be expected to trade current reproduction (initial egg load) for future reproduction (resulting in a low OI). A low OI would also enhance the prospects of locating suitable oviposition sites, due to the greater ability for dispersal from the natal site (see above).

The likelihood of locating suitable oviposition sites may also affect clutch size (laying eggs singly vs. as clusters of various sizes), and hence interact with OI. As far as is known, there are no insect-based studies contrasting the amount of time required for successful oviposition of a given number of eggs by single vs. cluster layers in similar habitats. If layers of single eggs are more likely to be time-limited, and layers of clusters more prone to egg limitation, then low and high OI respectively will be expected in these species.

The same predictions for the relationship between OI and the degree of polyphagy arise from the ‘time-limited disperser’ (TLD) model of optimal foraging theory. This predicts that individuals that can search for resources over a long period of time will specialise, whereas animals that have limited overall search times will generalise (Ward, 1986; Jaenike, 1990; Mayhew, 1997). These strategies would correspond to low OI and high OI respectively, given the negative correlation between OI and lifespan. Although the TLD model was formulated for the intraspecific level, Prinzing (2003) found strong support for it at the interspecific level using a variety of arthropods. An egg maturation-based dynamic programming model, developed by Roitberg (2000) for parasitoid wasps, predicts an inverse relationship between OI and degree of host discrimination, because of the relationship between OI and the relative degree of egg limitation.

Direct tests of these predictions are scarce. However, within Lepidoptera, the highly polyphagous, tree-feeding Geometridae in Table 1 have OIs of 1 or ≈ 1 (as do lymantriids, which are typically highly polyphagous), whereas the monophagous and narrowly polyphagous butterflies have OIs of 0 or ≈ 0, and sphingids (which are typically host-plant specialists) have OIs of <1. Additionally, laying of eggs in clusters tends to be found mainly among moths having an OI = 1 or ≈ 1, whilst among some butterflies, OI = 0 or ≈ 0 for single egg-layers, but is higher for most of the related species that lay eggs in clusters (Table 1).

Conclusions

Resource allocation has long been viewed as a basis for life-history trade-offs, with researchers generally considering just a pair of traits at any given time (e.g. Van Noordwijk & de Jong, 1986). The conceptual model that is presented here elaborates on this theme by proposing suites of traits, driven by integrated allocation patterns. It must be reiterated that allocation to reproduction prior to adult emergence (OI) was chosen as the key element around which to organise this review, not because it has necessarily driven the evolution of the suites of traits, but because it is a quantifiable, universal, and critical element of reproductive allocation for holometabolous insects.

The correlations discussed here, by themselves, cannot provide a complete understanding of functional trade-offs between the life-history traits of holometabolous insects. Trade-offs must be confirmed through physiological studies, especially those involving hormonal manipulation and/or nutrient-tracking techniques applied to individual species (see Zera & Harshman, 2001 for a discussion). The underlying genetic control is also of interest, and this would be investigated through selection and breeding experiments (see Roff, 2002 for a review).

Nonetheless, the results of this review should aid understanding of resource allocation rules not only among Lepidoptera but also among holometabolous insects generally. Currently, behavioural ecological models differ greatly in their assumptions regarding the partitioning of resources (e.g. see Jervis & Kidd, 1999; Casas et al., 2005). Additionally, by parameterising models, it is possible to explore how resilient particular life-history strategies are in maintaining high fitness under environmental variation of different kinds (see Boggs, 2003); it is possible, for example, that individuals are constrained from maximising their fitness under stressful conditions because allocation to one function takes precedence over allocation to another, i.e. a priority rule applies (see Zera & Harshman, 2001). Also, an explicit allocation-based understanding of the organisation of suites of life-history traits and their responses to variable environments, considered along with their connections to population dynamics (see A conceptual model of resource allocation and acquisition), can contribute significantly to population management strategies, either of pest or of endangered species.

Acknowledgements

We thank Malcolm Scoble for his advice at a very early stage in this study, and for imparting some of his immense knowledge of Lepidoptera; Jacintha Ellers, Matt Gage, Annette Herz, Jason Jannot, Simon Leather, Bill Miller, David Stevens, Rob Thomas, George Tordoff, and Christer Wiklund for valuable comments on drafts; David Stevens for allowing us to quote data from his doctoral research; Michael Braby, Melody Keena, Simon Leather, David Lees, George Tordoff, and Denis Wright for providing life-history information on some species; Chris Thomas for advice on dispersal characteristics of butterflies; Koen Berwaerts for discussing aspects of flight performance in Lepidoptera; Ilkka Hanski for access to his paper prior to its publication; Neil Kidd for useful discussions; and Craig Fee and Wendy Fox Knight for library assistance. We also owe a great debt not only to all the entomologists who gathered the primary data, but also to two pioneers of research into lepidopteran egg maturation and resource acquisition strategies: H. Eidmann and M. Norris.

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