Pollen feeding inHeliconiusbutterflies: the singular evolution of an adaptive suite

Abstract

Major evolutionary transitions can be triggered by behavioural novelty, and are often associated with ‘adaptive suites’, which involve shifts in multiple co-adapted traits subject to complex interactions. Heliconius butterflies represent one such example, actively feeding on pollen, a behaviour unique among butterflies. Pollen feeding permits a prolonged reproductive lifespan, and co-occurs with a constellation of behavioural, neuroanatomical, life history, morphological and physiological traits that are absent in closely related, non-pollen-feeding genera. As a highly tractable system, supported by considerable ecological and genomic data, Heliconius are an excellent model for investigating how behavioural innovation can trigger a cascade of adaptive shifts in multiple diverse, but interrelated, traits. Here, we synthesize current knowledge of pollen feeding in Heliconius , and explore potential interactions between associated, putatively adaptive, traits. Currently, no physiological, morphological or molecular innovation has been explicitly linked to the origin of pollen feeding, and several hypothesized links between different aspects of Heliconius biology remain poorly tested. However, resolving these uncertainties will contribute to our understanding of how behavioural innovations evolve and subsequently alter the evolutionary trajectories of diverse traits impacting resource acquisition, life history, senescence and cognition.

Balanced polymorphisms and their divergence in a Heliconius butterfly

“…erato and H . melpomene have an estimated dispersal range of only ~2.5–5 km (Mallet, 1986a ; Mallet et al, 1990 ), as a result of their “trap‐line” behaviors as adults (Young & Montgomery, 2020 ). However, it has been suggested that Heliconius doris may disperse much larger distances immediately post pupal eclosion, which could reduce chances of sib‐competition and sib‐matings (Mallet, 1999 ).…”

“…A possible explanation lies in the dispersal behavior from nearby populations where red co-mimics are present and the red H. doris morphs have greater protection. Other Heliconius species such as H. erato and H. melpomene have an estimated dispersal range of only ~2.5-5 km (Mallet, 1986a;Mallet et al, 1990), as a result of their "trapline" behaviors as adults (Young & Montgomery, 2020). However, it has been suggested that Heliconius doris may disperse much larger distances immediately post pupal eclosion, which could reduce chances of sib-competition and sib-matings (Mallet, 1999).…”

Divergence inHeliconiusflight behaviour is associated with local adaptation to different forest structures

“…Heliconius are also unique among butterflies for actively collecting and digesting pollen grains (Gilbert, 1972; Young & Montgomery, 2020) which may further predispose them to adaptive shifts in foraging behaviour. This adult source of amino acids is essential for extended longevity of female fecundity and reproductive output (Dunlap‐Pianka et al, 1977; O'Brien et al, 2003).…”

Pollen Feeding Reduces Predation of Northern Corn Rootworm Eggs (Coleoptera: Chrysomelidae, Diabrotica barberi) by a Soil-Dwelling Mite (Acari: Laelapidae: Stratiolaelaps scimitus)

“…Although pollen contains several secondary compounds [11,13,14,16,17], and sunflower pollen is rich in alkaloids [15,56], there are few studies indicating pollen is the source of chemoprotective chemicals for insects. Heliconius butterflies, which are unusual in that they consume pollen (including from plants within the Cucurbitaceae), contain cyanogenic glycosides and are more unpalatable than closely-related non-pollen feeding species [113,114], which is attributed to the pollen providing amino acids needed to biosynthesize the defensive compounds [115,116]. There is also the possibility that the field-collected pollen we fed to NCR adults was contaminated with pesticides, atmospheric pollutants [14,117], or other plant compounds, e.g., sesquiterpene lactones and diterpenes from sunflower glandular trichomes [118,119].…”