Why grow up? A perspective on insect strategies to avoid metamorphosis

Insects that have lost complete metamorphosis via type I paedomorphosis are known from several independent dipteran lineages and the beetle species Micromalthus debilis.

“Insects that have lost complete metamorphosis via type I paedomorphosis are known from several independent dipteran lineages (Johannsen, 1910; Wyatt, 1961, 1963, 1967; Ibrahim & Gad, 1975; Hodin & Riddiford, 2000) and the unusual beetle species Micromalthus debilis (reviewed in Pollock & Normark, 2002).”

• cites Johannsen, 1910 sourceNot checked — no full text of the source
• cites Wyatt, 1961 sourceNot checked — no full text of the source
• cites Pollock & Normark, 2002 sourcePartly supported

  The Life cycle section describes reproductive larvae of Micromalthus debilis that can produce young without pupating, supporting the beetle example. It also reports pupae and winged adults, so the paper does not support saying the species has lost complete metamorphosis altogether. The cited passage does not identify this process as “type I paedomorphosis”; the dipteran lineages have separate citations in the citing sentence. (LLM, conf=0.84)

  Experimental — accuracy not yet measured

Flies that have lost complete metamorphosis via type I paedomorphosis are most prominent among the more basally located dipteran clades, including Cecidomyiidae, Chironomidae and Syrphidae.

“Flies that have lost complete metamorphosis via type I paedomorphosis are most prominent among the more basally located dipteran clades (Wiegmann et al. , 2011), including the gall-midges, Cecidomyiidae (Wyatt, 1961, 1963, 1967), Chironomidae (Johannsen, 1910) and Syrphidae (Ibrahim & Gad, 1975; Achterkamp et al. , 2000).”

• cites Wiegmann et al., 2011 sourcePartly supported

  The Abstract describes a fly phylogeny and an early radiation of lower Diptera, supporting the general phylogenetic framing. It does not say that loss of complete metamorphosis through type I paedomorphosis is most prominent in basal clades, or establish that distribution for the named families. (LLM, conf=0.76)

  Experimental — accuracy not yet measured
• cites Wyatt, 1961 sourceNot checked — no full text of the source
• cites Johannsen, 1910 sourceNot checked — no full text of the source

Ovoviviparous insects, such as the termitophilous beetle Corotoca or certain flies, have minimised the role of metamorphosis by depositing larvae that are so developmentally advanced they are almost ready to pupate.

“For example, ovoviviparous insects, such as the termitophilous beetle Corotoca (Staphylinidae) or certain flies (Hippobscoidea), have minimised the role of metamorphosis by depositing larvae that are so developmentally advanced, they are almost ready to pupate [Crowson, 1981; Meier et al. , 1999 (citing Seevers, 1957)].”

• cites Crowson, 1981Not checked — no full text of the source
• cites Meier et al., 1999 sourcePartly supported

  The Abstract (p. 199) describes viviparity in flies, including shortened larval life and offspring deposited as pupae. But it defines ovoviviparity as depositing eggs from which larvae emerge immediately; it does not support calling the near-pupation larvae ovoviviparous, or the claim that metamorphosis is minimised. The passages found do not address Corotoca. (LLM, conf=0.82)

  Experimental — accuracy not yet measured

In holometabolous insects, a small increase in the expression of 20E in the absence of JH during the final larval instar induces pupal commitment, leading to epidermal expression of the transcription factor broad (br).

“In holometabolous insects, a small increase in the expression of 20E in the absence of JH during the final larval instar induces pupal commitment, leading to epidermal expression of the transcription factor broad ( br ) (Zhou & Riddiford, 2001).”

• cites Zhou & Riddiford, 2001 sourceSupported

A lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis.

“In contrast, no evidence of elevated br expression was observed for female X. vesparum , which do not enter the pupal stage and remain larviform at maturity, suggesting that a lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis (Erezyilmaz et al. , 2014).”

• cites Erezyilmaz et al., 2014 sourcePartly supported

  The Results report increased br expression in fourth-instar males but not females, and the Discussion suggests that loss of a switch in br expression may underlie neoteny in X. vesparum. The paper does not identify this developmental pattern as “type II paedomorphosis,” so that specific classification is not supported by our copy. (LLM, conf=0.82)

  Experimental — accuracy not yet measured

Amphitokous forms of Micromalthus debilis follow both the thelytokous and arrhenotokous pathways.

“Amphitokous forms follow both of the aforementioned pathways (Pollock & Normark, 2002).”

• cites Pollock & Normark, 2002 sourceSupported

No evidence of elevated br expression was observed for female Xenos vesparum, which do not enter the pupal stage and remain larviform at maturity.

“In contrast, no evidence of elevated br expression was observed for female X. vesparum , which do not enter the pupal stage and remain larviform at maturity, suggesting that a lack of br up-regulation may underlie loss of complete metamorphosis via type II paedomorphosis (Erezyilmaz et al. , 2014).”

• cites Erezyilmaz et al., 2014 sourceSupported

Some risk likely accompanies the maintenance of beneficial over detrimental (pathogenic) symbiotic interactions while the gut lining is renewed during pupation.

“Additionally, it is likely that some risk must accompany the maintenance of beneficial over detrimental (i.e. pathogenic)”

• cites Johnston & Rolff, 2015 sourceSupported

Defensive coloration and luminescence represent ancestral aposematic traits of other paedomorphic elateroid lineages such as Lampyridae and Phengodidae.

“Interestingly, defensive coloration (Linsley et al. , 1961) and luminescence (De Cock & Matthysen, 2001) represent ancestral aposematic traits of other paedomorphic elateroid lineages such as Lampyridae and Phengodidae (Bocak et al. , 2008).”

• cites Linsley et al., 1961 sourceNot checked — no full text of the source
• cites De Cock & Matthysen, 2001 sourceNot checked — no full text of the source
• cites Bocak et al., 2008 sourcePartly supported

  The Discussion (section 4) identifies luminescence as an aposematic signal in Lampyridae and Phengodidae and says these defensive strategies preceded the shift to extreme neoteny. It assigns aposematic coloration to Cantharidae and Lycidae, however, not to Lampyridae or Phengodidae, so the claim’s grouping of both traits with the latter lineages is not fully supported. (LLM, conf=0.85)

  Experimental — accuracy not yet measured

In M. debilis, as an alternative to all-female diploid broods (approximately 10 daughters), the mother larva can produce a single haploid son that consumes the mother before pupating into a fully metamorphosed adult.

“In M. debilis (Micromalthidae), as an alternative to all female diploid broods (approx. 10 daughters), the mother larva can also produce a single haploid son that consumes the mother before pupating into a fully metamorphosed adult.”

• cites Pollock & Normark, 2002 sourceSupported

For many groups, such as Scarelus or Telegeusidae, while extreme paedomorphosis and total avoidance of pupation are suspected, the exact status of pupation and the putative terminal stage when females attain reproductive maturity remain unknown.

“Unfortunately, for many groups, such as Scarelus (Lycidae) (Malohlava & Bocak, 2011) or the Telegeusidae (Jeng, 2008), while extreme paedomorphosis and total avoidance of pupation are suspected, the exact status of pupation and the putative terminal stage when females attain reproductive maturity remain unknown.”

• cites Malohlava & Bocak, 2011 sourcePartly supported

  Split into 2 atoms — 0 confirmed, 2 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.

  Experimental — accuracy not yet measured
• cites Jeng, 2008Not checked — no full text of the source

In Strepsiptera and phylogenetically well-resolved elateroid beetles, the trade-off between dispersal and fecundity appears to be total, with no reversals apparent across phylogeny.

“In Strepsiptera (McMahon et al. , 2011a) and phylogenetically well-resolved elateroid beetles (e.g. Lycidae; Bocak et al. , 2008; Masek et al. , 2015), the trade-off appears to be total (no reversals are apparent across phylogeny; although see Jeng, 2008 for a wider discussion of Elateroidea).”

• cites McMahon et al., 2011aNot matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

• cites Bocak et al., 2008 sourcePartly supported

  The Discussion reports that wing loss reduces dispersal in neotenic Lycidae while allowing greater investment in reproduction, and says trait mapping is consistent with no reversals in neoteny. It also describes these changes as stepwise, rather than establishing a total dispersal–fecundity trade-off. This citation supports the Lycidae portion of the sentence, not the separately cited Strepsiptera portion. (LLM, conf=0.82)

  Experimental — accuracy not yet measured
• cites Masek et al., 2015 sourcePartly supported

  The Introduction (page unavailable) links wingless, larviform females in Lycidae to very limited dispersal and describes their investment in a relatively small number of large eggs. The Discussion (page unavailable) presents a phylogeny of these beetles, but the paper does not establish that the dispersal–fecundity trade-off is total or that no evolutionary reversals occurred. This verdict concerns the elateroid-beetle portion attributed to Masek et al., not the separately cited Strepsiptera portion. (LLM, conf=0.85)

  Experimental — accuracy not yet measured

A total lack of metamorphosis via type II paedomorphosis is strongly suspected in at least three other lineages within the Lycidae alone.

“Outside of the Platerodrilini, a total lack of metamorphosis via type II paedomorphosis is strongly suspected in at least three other lineages within the Lycidae alone (Levkanicova & Bocak, 2009; Malohlava & Bocak, 2011; Masek et al. , 2014).”

• cites Levkanicova & Bocak, 2009 sourceNot checked — no full text of the source
• cites Malohlava & Bocak, 2011 sourcePartly supported

  The Natural history section (page unavailable) says the authors suspect sexually mature Ateliini females remain larviform, but that female neoteny has not been proven by observation. This supports Ateliini as one suspected lycid lineage outside Platerodrilini; the paper does not establish a total lack of metamorphosis, identify it as type II paedomorphosis, or substantiate the count of at least three lineages. (LLM, conf=0.85)

  Experimental — accuracy not yet measured
• cites Masek et al., 2014 sourceNot checked — no full text of the source

Very limited ancestral ranges for Platerodrilus beetles, together with nutrient-poor diet and sedentary anti-predatory adaptations, could exacerbate a dispersal-reproduction trade-off due to reduced incentives to disperse.

“Together with what are thought to be very limited ancestral ranges for Platerodrilus beetles (Masek et al. , 2015), such factors could exacerbate a disperal reproduction-based trade off, due to reduced incentives to disperse (Zera & Harshman, 2001).”

• cites Masek et al., 2015 sourceSupported
• cites Zera & Harshman, 2001 sourceNot checked — no full text of the source

In platerodrilid lycid beetles, long developmental times and inactivity are characteristic of females.

“In platerodrilid lycid beetles (Elateroidea), long developmental times and inactivity are characteristic of females (Bocak et al. , 2008).”

• cites Bocak et al., 2008 sourceSupported

Within Holometabola, only females have lost the ability to completely metamorphose.

“Within Holometabola, only females have lost the ability to completely metamorphose.”

• Also stated in: § Why grow up? A perspective on insect strategies to avoid metamorphosis · p. 1 · plain

  “Interestingly, only female holometabolous insects have entirely avoided complete metamorphosis, and it is always the ancestrally juvenile morphology that is retained.”

Females with type I paedomorphosis are characterised by the ability to facultatively 'choose' to undergo complete metamorphosis, or not, as part of a mixed life cycle strategy that contains both metamorphic and paedomorphic cycles.

“Here, females are characterised by the ability to facultatively 'choose' to undergo complete metamorphosis, or not, as part of a mixed life cycle strategy that contains both metamorphic and paedomorphic cycles.”

The loss of complete metamorphosis has occurred repeatedly, originating independently several times in divergent lineages distributed across three holometabolous insect orders.

“We found that the loss of complete metamorphosis has occurred repeatedly, originating independently several times in divergent lineages distributed across three holometabolous insect orders.”

• Also stated in: § Why grow up? A perspective on insect strategies to avoid metamorphosis · p. 1 · plain

  “While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described.”

With respect to holometabolous insects that have entirely lost complete metamorphosis, this has only occurred in females, where it has been achieved via the deletion of the pupal and post-metamorphic stage (the ancestral adult), via paedomorphosis.

“With respect to holometabolous insects that have entirely lost complete metamorphosis, this has only occurred in females, where it has been achieved via the deletion of the pupal and post-metamorphic stage (i.e. the ancestral 'adult'), via a developmental process known as paedomorphosis.”

In females that have lost complete metamorphosis, the larval stage is retained and reproductive maturity is differentiated by the development of sexual traits (germ line and genitalia) without progression to a discrete pupal stage or a metamorphic terminal imago.

“Specifically, the larval stage is retained and reproductive maturity is differentiated by the development of sexual traits (i.e. the development of the germ line and genitalia) without progression to a discrete pupal stage or a metamorphic terminal imago.”

Complete metamorphosis is retained in males in both type I and type II strategies.

“A further difference from type I species is that complete metamorphosis cannot be facultatively regained in type II females in response to external environmental cues, although as is common to both strategies, it is retained in males.”

In type I paedomorphosis, reproduction is parthenogenetic.

“Common to all insects possessing this strategy, development and maturation of the germ line are accelerated and occur during the larval stage, resulting in arrested development of the soma, no further bodily growth, and parthenogenetic reproduction.”

In type II paedomorphosis, development of the genitalia continues into an undifferentiated terminal stage.

“but development of the genitalia continues into an undifferentiated terminal stage”

Diptera contain possibly the highest number of known independent evolutionary losses of metamorphosis via type I paedomorphosis.

“Diptera contain possibly the highest number of known independent evolutionary losses of metamorphosis via type I paedomorphosis.”

In all insects possessing type I paedomorphosis, development and maturation of the germ line are accelerated and occur during the larval stage.

“Common to all insects possessing this strategy, development and maturation of the germ line are accelerated and occur during the larval stage, resulting in arrested development of the soma, no further bodily growth, and parthenogenetic reproduction.”

In type II females, complete metamorphosis cannot be facultatively regained in response to external environmental cues.

“A further difference from type I species is that complete metamorphosis cannot be facultatively regained in type II females in response to external environmental cues, although as is common to both strategies, it is retained in males.”

Some insects have minimised or even lost the holometabolous lifestyle, at least from some part of the life cycle.

“Yet despite the apparent virtues of holometaboly, some insects have minimised or even lost the holometabolous lifestyle, at least from some part of the life cycle.”

In type II paedomorphosis, the rate of maturation of the germ line continues normally, which permits extended body growth.

“Importantly, instead of an associated acceleration of germ line development as in type I paedomorphosis, the rate of maturation of the germ line continues normally, which, unlike in type I paedomorphosis, permits extended body growth.”

Known independent losses of complete metamorphosis are highly uneven in taxonomic distribution, with a conservatively estimated minimum of four, four and one independent losses in Diptera, Coleoptera and Strepsiptera, respectively.

“Nonetheless, known independent losses are highly uneven in their taxonomic distribution, with a conservatively estimated minimum of four, four and one independent losses in Diptera, Coleoptera and Strepsiptera, respectively (Table 1).”

In insects that have lost metamorphosis via type II paedomorphosis, development of the soma is terminated during or at the end of the larval stage.

“In insects that have lost metamorphosis via type II paedomorphosis, development of the soma is also terminated during or at the end of the larval stage (Cicero, 1988; Jeng, 2008)”

• cites Cicero, 1988Not matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

• cites Jeng, 2008Not checked — no full text of the source

In gall midges such as Mycophila speyeri, larval parthenogenesis proceeds via viviparous thelytoky, with mothers giving birth to live all-female progeny initially developing from unfertilised eggs.

“In gall midges such as Mycophila speyeri (Fig. 1a), larval parthenogenesis proceeds via viviparous thelytoky, i.e. mothers give birth to live all-female progeny initially developing from unfertilised eggs (Hodin & Riddiford, 2000; Normark, 2003).”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source
• cites Normark, 2003 sourceNot checked — no full text of the source

A minimum number of three losses of complete metamorphosis within Elateroidea have occurred independently (Lycidae, Phengogidae + Rhagophthalmidae and Lampyridae).

“Taking these uncertainties into account, a minimum number of three losses of complete metamorphosis within Elateroidea have occurred independently (Lycidae, Phengogidae + Rhagophthalmidae and Lampyridae).”

In the thelytokous form of Micromalthus debilis, multiple female offspring are produced via viviparity inside the larval mother.

“In the thelytokous form, multiple female offspring are produced via viviparity inside the larval mother.”

Unlike type I species, the sexes in type II species are permanently dimorphic for complete metamorphosis (males undergo complete metamorphosis, while females do not).

“Unlike type I species, the sexes in type II species are permanently dimorphic for complete metamorphosis (i.e. males undergo complete metamorphosis, while females do not).”

Micromalthus debilis is haplodiploid.

“M. debilis is haplodiploid (Scott, 1938), whereas cecidomyiids, as in some sciarid dipterans and scale insects, have an unusual form of paternal chromosome elimination (Stuart & Hatchett, 1991), whereby males have no influence on the sex of the progeny (Stuart & Hatchett, 1988).”

• cites Scott, 1938 sourceNot checked — no full text of the source

The trigger for switching between parthenogenesis in larval forms or sexual reproduction in normal adults in gall midges is ecological.

“The trigger for switching between parthenogenesis in larval forms or sexual reproduction in normal adults is an ecological one.”

Type I species are characterised (but not necessarily defined) by atypical genetic systems.

“Type I species are also characterised (but not necessarily defined) by atypical genetic systems.”

Loss of complete metamorphosis via type I paedomorphosis is characterised by a mixed life cycle strategy composed of short parthenogenetic cycles and longer dispersive sexual cycles.

“Conversely, loss of complete metamorphosis via type I paedomorphosis is characterised by a mixed life cycle strategy composed of short parthenogenetic cycles and longer dispersive sexual cycles.”

The final stage of Platerodrilus ruficollis differs from the previous larval stage only in the development of the genitalia.

“It corroborates Mjöberg (1925) in stating that the final stage differs from the previous larval stage only in the development of the genitalia and describes the first successful mating of lycids in the laboratory (although the hatched larvae subsequently died).”

• cites Wong, 1996Not matched

  Couldn’t be matched to a paper in Crossref, so it can’t be checked.

• cites Mjöberg, 1925 sourceNot checked — no full text of the source

In female Strepsiptera, further gross modifications to the body cease at the fourth larval instar, except in relation to the formation and extrusion of the cephalothorax through the host cuticle.

“Further gross modifications to the body cease at the fourth larval instar in females, except in relation to the formation and extrusion of the cephalothorax through the host cuticle.”

The richest diversity and best understood examples of type I paedomorphosis in holometabolous insects come from the Cecidomyiidae.

“The richest diversity and best understood examples of type I paedomorphosis in holometabolous insects come from the Cecidomyiidae.”

Among derived families of Strepsiptera, in genera such as Xenos, male and female development is similar until the fourth larval instar.

“Among the derived families of the order Strepsiptera (the so called 'twisted-wing parasites'), in genera such as Xenos , male and female development is similar until the fourth larval instar (Beani et al. , 2005).”

• cites Beani et al., 2005 sourceNot checked — no full text of the source

In the arrhenotokous form of Micromalthus debilis, females produce a single male egg, giving rise to a larva that subsequently cannibalises the mother and grows over several instars before undergoing complete metamorphosis to become a dispersive adult.

“In the arrhenotokous form, females produce a single male egg, giving rise to a larva that subsequently cannibalises the mother and grows over several instars before undergoing complete metamorphosis to become a dispersive adult (Scott, 1938).”

• cites Scott, 1938 sourceNot checked — no full text of the source

Individual parthenogenetic female larvae of Micromalthus debilis are either thelytokous, arrhenotokous or amphitokous.

“Individual parthenogenetic female larvae are either thelytokous, arrhenotokous or amphitokous.”

Extrusion of the cephalothorax in Strepsiptera is timed to coincide with eclosion of winged adult males.

“Extrusion of the cephalothorax is timed to coincide with eclosion of winged adult males (Hrabar et al. , 2014).”

• cites Hrabar et al., 2014 sourceNot checked — no full text of the source

Several lineages have evolved life cycle modifications to avoid complete metamorphosis.

“Yet holometaboly can also impose costs, and several lineages have evolved life cycle modifications to avoid complete metamorphosis.”

In common with Strepsiptera, females from several distant elateroid lineages have permanently lost metamorphosis.

“However, in common with Strepsiptera, females from several distant elateroid lineages have permanently lost metamorphosis.”

Only a small number of species possessing the ability to lose complete metamorphosis in females have been described.

“While the loss of complete metamorphosis in females has occurred independently on several occasions across holometabolous insects, only a small number of species possessing this ability have been described.”

Extremely paedomorphic lineages of Strepsiptera and Elateroidea harbour many hundreds of species, compared with just a handful of described cecidomyiid species and the single beetle M. debilis.

“Extremely paedomorphic lineages of Strepsiptera and Elateroidea harbour many hundreds of species compared with just a handful of described cecidomyiid species and the single beetle M. debilis .”

• AssumptionRests on an assumption: The compiled taxonomic distribution and species counts of paedomorphic lineages (Table 1) accurately reflect the true diversity and phylogenetic distribution of these lineages.

Each transition to the loss of complete metamorphosis involved the evolution of a highly derived reproduction-competent larva, rather than a reversion to hemimetabolous development.

“Furthermore, each transition involved the evolution of a highly derived reproduction-competent larva, rather than a reversion to hemimetabolous development.”

• AssumptionRests on an assumption: The compiled taxonomic distribution and species counts of paedomorphic lineages (Table 1) accurately reflect the true diversity and phylogenetic distribution of these lineages.

The loss of complete metamorphosis from ancestrally holometabolous females does not feature a reversal to hemimetaboly, but instead represents a derived state of holometaboly with incomplete larval development.

“Importantly, the loss of complete metamorphosis from ancestrally holometabolous females does not feature a reversal to hemimetaboly, but instead represents a derived state of holometaboly with incomplete larval development.”

Holometaboly appears to have been a key innovation in the most successful radiation of animals during evolutionary history.

“Thus, holometaboly appears to have been a key innovation in the most successful radiation of animals during evolutionary history.”

The transition to complete metamorphosis is evolutionarily irreversible.

“This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.”

Significant modifications to the holometabolan metamorphic ground plan are highly constrained.

“This indicates that significant modifications to the holometabolan metamorphic ground plan are highly constrained, and suggests that the transition to complete metamorphosis is evolutionarily irreversible.”

Most animal species undergo some form of metamorphosis.

“A focus on the adult stage and the neglect of others is undermined by knowledge that most animal species undergo some form of metamorphosis (Werner, 1988), and that complex life cycles composed of discrete developmental stages - and associated shifts in ecology - are the norm (Moran, 1994).”

• cites Werner, 1988 sourceNot checked — no full text of the source

Complete metamorphosis confers significant advantages because it enables organisms to optimise life-history components through temporal partitioning, and thereby to exploit multiple ecological niches.

“Complete metamorphosis confers significant advantages because it enables organisms to optimise life-history components through temporal partitioning, and thereby to exploit multiple ecological niches.”

Complex life cycles composed of discrete developmental stages and associated shifts in ecology are the norm.

“A focus on the adult stage and the neglect of others is undermined by knowledge that most animal species undergo some form of metamorphosis (Werner, 1988), and that complex life cycles composed of discrete developmental stages - and associated shifts in ecology - are the norm (Moran, 1994).”

• cites Moran, 1994 sourceNot checked — no full text of the source

These findings point to a strong sex-biased trade-off between investment in reproduction and development.

“These findings point to a strong sex-biased trade-off between investment in reproduction and development.”

Complete metamorphosis appears to have been almost fully retained.

“Thus, complete metamorphosis, which originated only once in insects, appears to have been almost fully retained.”

It is more likely that loss of complete metamorphosis within Elateroidea originated at least eight or nine times when strongly suspected cases in poorly characterised and/or equivocally positioned lineages are considered.

“This is a very conservative estimate, and it is more likely to have originated at least eight or nine times when the strongly suspected cases in poorly characterised and/or equivocally positioned elateroid lineages are considered.”

Holometabolous insects are extremely successful in measures of abundance, ecological function or species richness.

“Whether relating to measures of abundance, ecological function or species richness, holometabolous insects are extremely successful (Whiting, 2004).”

• cites Whiting, 2004 sourceNot checked — no full text of the source

Loss of complete metamorphosis by type I development has evolved at least twice in Cecidomyiidae.

“Although the exact phylogenetic relationships among cecidomyiid genera remain uncertain, it is reasonable to conclude that loss of complete metamorphosis by type I development has evolved at least twice in Cecidomyiidae.”

Paedomorphic reproduction is likely to be especially favoured in females because of the relative enhancement of fecundity (and therefore fitness) that accompanies the avoidance of a costly metamorphic stage.

“It is worth noting that paedomorphic reproduction is likely to be especially favoured in females because of the relative enhancement of fecundity (and therefore fitness) that accompanies the avoidance of a costly metamorphic stage.”

Indirect support in Strepsiptera comes from evidence of female-driven host associations following the transition from a small (ant) to a large (dictyopteran) host in the Myrmecolacidae.

“Indirect support in Strepsiptera comes from evidence of female-driven host associations following the transition from a small (ant) to large (dictyopteran) host in the Myrmecolacidae (Hayward et al. , 2011).”

• cites Hayward et al., 2011 sourceNot checked — no full text of the source

A number of other holometabolous species in similar habitats have evolved modified life cycles and a tendency towards both parthenogenesis and paedomorphosis, although never to the extent that complete metamorphosis is entirely avoided.

“To accommodate both sedentary and dispersive strategies, a number of other holometabolous species in similar habitats have evolved modified life cycles and a tendency towards both parthenogenesis and paedomorphosis (although never to the extent that complete metamorphosis is entirely avoided).”

There may be benefits gained by avoiding a pupal and terminal moult that outweigh the cost of being deprived of a diverse suite of holometabolous adult traits.

“However, there may also be benefits gained by avoiding a pupal and terminal moult that may outweigh the cost of being deprived of a diverse suite of holometabolous adult traits.”

In Drosophila melanogaster, EcR and USP are up-regulated only in the final larval stage.

“In Drosophila melanogaster , EcR and USP are up-regulated only in the final larval stage (Hodin & Riddiford, 1998).”

• cites Hodin & Riddiford, 1998 sourceNot checked — no full text of the source

Males are costly because a single son consumes the mother.

“Males are costly because a single son consumes the mother.”

The positive correlation between paedomorphosis and life cycle plasticity points to an advantage of maintaining a fully metamorphosed flight-capable adult stage somewhere in the life cycle.

“Furthermore, the positive correlation between paedomorphosis and life cycle plasticity points to an advantage of maintaining a fully metamorphosed flight-capable adult stage somewhere in the life cycle.”

In type I paedomorphosis, gall midges have evolved an alternative strategy involving early up-regulation of ecdysone receptor (EcR) and ultraspiracle (USP) in the ovaries.

“In type I paedomorphosis, gall midges have evolved an alternative strategy involving early up-regulation of ecdysone receptor (EcR) and ultraspiracle (USP) in the ovaries.”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source

The pupa, being an entirely sessile stage, is vulnerable to attack from a multitude of predators and parasitoids.

“Meanwhile, as an entirely sessile stage, the pupa is vulnerable to attack from a multitude of predators and parasitoids (Godfray, 1994).”

• cites Godfray, 1994 sourceNot checked — no full text of the source

When fresh fungal hyphae are present (high-quality food), up-regulation of EcR and USP occurs early in the first larval instar, leading to paedomorphic development.

“However, when fresh fungal hyphae are present (high-quality food), up-regulation of EcR and USP occurs early in the first larval instar, leading to paedomorphic development (Hodin & Riddiford, 2000).”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source

A major step in the loss of complete metamorphosis in Strepsiptera involved a transition to complete female endoparasitism.

“A major step in the loss of complete metamorphosis in Strepsiptera involved a transition to complete female endoparasitism.”

The loss of complete metamorphosis may be more common than is currently appreciated.

“Given the lack of knowledge concerning the pre-pupal biology of most insects (Hodin & Riddiford, 2000), which can be both highly cryptic (Kathirithamby & Johnston, 2004) and difficult to study (Mjöberg, 1925), the loss of complete metamorphosis may be more common than is currently appreciated.”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source
• cites Kathirithamby & Johnston, 2004 sourceNot checked — no full text of the source
• cites Mjöberg, 1925 sourceNot checked — no full text of the source

In type I paedomorphic species, the ephemeral nature of the high-quality resource patches on which they feed may favour a shortened life cycle.

“In type I paedomorphic species, the ephemeral nature of high-quality resource patches on which they feed may favour a shortened life cycle (Fig. 3a).”

The pattern of precocious up-regulation of EcR and USP is highly similar in both species of paedomorphic gall midge so far examined (Heteropeza pygmaea and Mycophila speyeri), despite the proposed convergent evolution of type I paedomorphosis in these species.

“Interestingly, the pattern of precocious up-regulation of EcR and USP is highly similar in both species of paedomorphic gall midge so far examined ( Heteropeza pygmaea and Mycophila speyeri ), despite the proposed convergent evolution of type I paedomorphosis in these species (Hodin & Riddiford, 2000).”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source

In gall midges with the capacity for paedomorphosis, when available fungal hyphae are old (low-quality food), EcR and USP up-regulation occurs only in the final larval stage and the flies undergo metamorphosis.

“This is also the case in gall midges with the capacity for paedomorphosis, when available fungal hyphae are old (low-quality food) and flies undergo metamorphosis (Hodin & Riddiford, 2000).”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source

The basis of the trade-off between dispersal and fecundity is similar to that in many other insect groups in which females have evolved vestigial adult traits such as reduced wings.

“We argue that the basis of the trade-off is similar to many other insect groups in which females have evolved vestigial adult traits such as reduced wings.”

In the Sciaridae, Plastosciara perniciosa is able to produce sexual micropterous larviform males and females as a facultative response to temporarily favourable environmental conditions.

“In the Sciaridae (Diptera), Plastosciara perniciosa is able to produce sexual micropterous larviform males and females as a facultative response to temporarily favourable environmental conditions (Steffan, 1973).”

• cites Steffan, 1973 sourceNot checked — no full text of the source

Increased body size during the transition to endoparasitism has been documented in other arthropods, such as copepods, where it is accompanied by a steady increase in parasite body size.

“Increased body size during the transition to endoparasitism has been documented in other arthropods, such as copepods, where it is accompanied by a steady increase in parasite body size (Poulin, 1995).”

• cites Poulin, 1995 sourceNot checked — no full text of the source

In Strepsiptera, the presence of motile planidial first larvae is probably essential in enabling complete female endoparasitism, because a larviform female would both lack oviposition apparatus and the ability to control egg-laying whilst constrained inside the host.

“In Strepsiptera, the presence of motile planidial first larvae is probably essential in enabling complete female endoparasitism, because a larviform female would both lack oviposition apparatus and the ability to control egg-laying whilst constrained inside the host.”

The rare occurrence of planidia, alongside a parasitoid-driven strategy centring on host immobilisation and rapid depletion of resources, could explain why parasitic Hymenoptera have never lost complete metamorphosis.

“The rare occurrence of planidia, alongside a parasitoid-driven strategy centring on host immobilisation and rapid depletion of resources, could explain why parasitic Hymenoptera have never lost complete metamorphosis.”

While a larval lifestyle appears highly adaptive, in holometabolous insects it occurs as just one component of a more complex life cycle.

“While a larval lifestyle appears highly adaptive, in holometabolous insects it occurs as just one component of a more complex life cycle.”

Specific pre-adaptations may be required for paedomorphosis that not all insects possess or can easily evolve.

“This indicates that specific pre-adaptations may be required for paedomorphosis that not all insects possess or can easily evolve.”

In the typical insect pattern, including the higher flies, ovarian somatic cell types differentiate before the germ line.

“This is in contrast to the typical insect pattern, including the higher flies, where ovarian somatic cell types differentiate before the germ line (Hodin & Riddiford, 2000).”

• cites Hodin & Riddiford, 2000 sourceNot checked — no full text of the source

The high phenotypic plasticity demonstrated by type I species may act as a brake on adaptive evolution and diversification, because highly plastic populations are likely to persist easily and undergo less genetic change.

“It is possible that the high phenotypic plasticity demonstrated by type I species may act as a brake on adaptive evolution and diversification, because highly plastic populations are likely to persist easily and undergo less genetic change (Price et al. , 2003; Pfennig et al. , 2010).”

• cites Price et al., 2003 sourceNot checked — no full text of the source
• cites Pfennig et al., 2010 sourceNot checked — no full text of the source