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Nymphalidae: Ithomiini) Butterflies from North-Eastern Peru

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Nymphalidae: Ithomiini) Butterflies from North-Eastern Peru Zoological Journal of the Linnean Society, 2016. With 4 figures Ecology, life history, and genetic differentiation in Neotropical Melinaea (Nymphalidae: Ithomiini) butterflies from north-eastern Peru MELANIE MCCLURE* and MARIANNE ELIAS Institut de Systematique, Evolution, Biodiversite, ISYEB – UMR 7205 – CNRS, MNHN, UPMC, EPHE, Museum National d’Histoire Naturelle, Sorbonne Universites, 57 rue Cuvier, CP50, F-75005 Paris, France Received 22 December 2015; revised 11 March 2016; accepted for publication 16 March 2016 Butterflies of the genus Melinaea have conspicuous warning colours and are thought to be the prime distasteful models in many cases of mimicry in the Neotropics. Colour pattern variability has made systematics challenging and previous studies have found little to no genetic differentiation. This paper provides detailed descriptions of the immature stages of seven Melinaea taxa from north-eastern Peru, including distribution and host plant use, in addition to measures of genetic differentiation using microsatellite markers and mitochondrial sequences. Development time and immature stages were similar, making it difficult to elucidate taxonomy based on larval morphological characters. All taxa used Juanulloa as a host plant (Solanaceae), except Melinaea ‘marsaeus’ mothone, which occurs at higher elevations and used Trianaea (Solanaceae). The seven taxa show virtually no mitochondrial divergence, suggesting a recent radiation. Microsatellite markers, however, revealed distinct genetic clusters and evidence of admixture, demonstrating a complex diversification history. Ecological and genetic differentiation observed for Mel. ‘marsaeus’ mothone prompts for a taxonomic status revision to Melinaea mothone mothone and the taxonomic status of Melinaea ‘satevis’ tarapotensis remains unclear. Clearly, further work is needed to clarify the systematics and to shed light on the processes driving speciation in this genus. © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016 doi: 10.1111/zoj.12433 ADDITIONAL KEYWORDS: aposematic – Danainae – development – distribution – host plants – Lepi- doptera – mimicry – morphology – Solanaceae – taxonomy. and mimicry (Whinnett et al., 2005; Dasmahapatra INTRODUCTION et al., 2010), and offer an excellent system to study Mullerian€ mimicry, where multiple unpalatable spe- the mechanisms underlying diversification. These cies possess the same warning signal, reduces the butterflies are large, possess conspicuous aposematic negative impact of predation on each species by shar- warning colours, and are distributed across much of ing the cost of educating predators. Mimetic butter- the Neotropics. They are also extensively involved in flies are well suited for studies on speciation, as mimicry rings, including with ‘tiger-patterned’ species often consist of multiple subspecies diverging (black, orange, and yellow) Heliconius, and are for a number of adaptive traits, such as colour pat- thought to drive mimicry in many other Lepidoptera tern, which can then cause reproductive isolation (Brown & Benson, 1974; Beccaloni, 1997). However, through sexual selection and higher hybrid mortality their colour pattern variability and the lack of mor- (Jiggins et al., 2001; Merrill et al., 2012). Butterflies phological differentiation have presented taxonomical in the genus Melinaea (Nymphalidae: Ithomiini) challenges, and consequently the systematics of this have undergone rapid radiation for warning patterns genus remains unclear (Brown, 1977). Previous stud- ies using mitochondrial and nuclear markers have *Corresponding author. E-mail: [email protected] found little to no genetic differences amongst many © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016 1 2 M. MCCLURE AND M. ELIAS species of Melinaea, and it is postulated that they general, are extremely difficult to keep and breed in have only recently diverged (Whinnett et al., 2005; cages, owing to specific ecological requirements such Elias et al., 2007; Dasmahapatra et al., 2010). as shaded habitat and plants that provide precursors In other groups of aposematic and mimetic butter- of sexual pheromones. Therefore, mating behaviour flies, detailed descriptions of the life history and of is poorly documented in these species. the immature stages have revealed distinguishing The few scattered records of host-plant use that ecological and morphological characteristics useful exist suggest that Melinaea species are oligophagous for resolving such taxonomic issues (Brown & Fre- on the family Solanaceae, subclade Juanulloeae (see itas, 1994; Hill et al., 2012). Yet, despite Melinaea Table 1). For example, Melinaea lilis has been butterflies being the prime distasteful models in recorded on Merinthopodium neuranthum and Mar- many cases of mimicry and interesting organisms for kea (Dyssochroma) viridiflora in Costa Rica, and on the study of speciation, general biological and life- Juanulloa mexicana in both Costa Rica and Mexico history information for this genus are still lacking. (see Brown & Freitas, 1994; Drummond & Brown, Reasons for the paucity of life-history information 1987). Melinaea menophilus has been recorded on include the difficulty of finding the host-plants of Markea (Hawkesiophyton) ulei in Brazil (Drummond Melinaea species, which are mostly epiphytes & Brown, 1987; Brown & Freitas, 1994), and on Mar- (Knapp, Persson & Blackmore, 1997). In addition, kea sp. (Willmott & Mallet, 2004), J. mexicana Melinaea species, and ithomiine butterflies in (Drummond & Brown, 1987), and Juanulloa Table 1. Records of host plants for Melinaea, including the country and the altitude at which it was recorded, when available, and the reference from where it was taken. Melinaea species Host plant Locality Altitude References Melinaea mneme mneme Markea coccinea Brazil 50–100 m Drummond & Brown (1987) Melinaea mneme mauensis Markea coccinea Brazil 10 m Drummond & Brown (1987) Melinaea ludovica ludovica Markea sp. Brazil 20 m Drummond & Brown (1987) Melinaea ludovica paraiya Markea (Dyssochroma) Brazil Sea level–800 m, Drummond & Brown viridiflora 20–300 m (1987) Melinaea lilis imitata Juanulloa mexicana Mexico, 200–1600 m, sea Drummond & Brown Costa Rica level–1600 m (1987) Melinaea lilis imitata Merinthopodium Costa Rica Sea level–1600 m Drummond & Brown neuranthum (1987) Melinaea lilis imitata Solandra grandiflora Costa Rica Sea level–1600 m Drummond & Brown (1987) Melinaea lilis parallelis Markea (Schultesianthus) Panama Sea level–2000 m Drummond & Brown leucantha (1987) Melinaea marsaeus pothete Markea (Hawkesiophyton) Brazil 200–600 m Drummond & Brown ulei (1987) Melinaea menophilus Juanulloa mexicana Ecuador 280 m Drummond & Brown menophilus (1987) Melinaea menophilus Markea (Hawkesiophyton) Brazil 200–600 m Drummond & Brown ssp. nov. ulei (1987) Melinaea lilis Juanulloa mexicana Mexico Brown & Freitas (1994) Melinaea menophilus Markea (Hawkesiophyton) Brazil Brown & Freitas (1994) ulei Melinaea ludovica paraiya Markea (Dyssochroma) Brazil Brown & Freitas (1994) viridiflora Melinaea ethra Markea (Dyssochroma) Brazil Brown & Freitas (1994) viridiflora Melinaea menophilus Juanulloa ochracea Ecuador K. Willmott, pers. comm. Melinaea mneme mauensis Markea formicarum French 50–100 m M. McClure, pers. observ.; Guiana Fig. S2 Melinaea menophilus zaneka Markea sp. Ecuador Montane Willmott & Mallet (2004) © 2016 The Linnean Society of London, Zoological Journal of the Linnean Society, 2016 DIFFERENTIATION IN MELINAEA BUTTERFLIES 3 ochracea (K. Willmott, pers. comm.; see Fig. S1E) in collected in proximity to streams and water, confirm- Ecuador. Similarly, Melinaea mneme has been ing Melinaea’s association with humid habitats. Host recorded on Markea coccinea in Brazil (Drummond & plants were also frequently encountered in very Brown, 1987), and M. M. has also successfully reared humid habitats, often near streams and rivers, and Melinaea mneme mauensis on the ant-garden epi- eggs and larvae were found on those plants that were phyte Markea formicarum in French Guiana, despite accessible. Host plants were photographed and botan- it never having been observed to be used in the field ical samples were collected and then dried in silica gel (M. McClure, pers. observ., see Fig. S2). Shifts in or pressed before identification. host-plant usage have been shown to be a major Gravid wild-caught females were placed in cause of diversification in butterflies (Janz, Nylin & 2 9 2 9 2 m outdoor insectaries in Tarapoto, San Wahlberg, 2006; Nylin, Slove & Niklas, 2014). As Martın, where all rearing was carried out. These switches in host plants may be accompanied by cages were in the shade of nearby trees and made of changes in microhabitats and mimicry rings (Will- shade cloth that blocked 50% of sunlight, so as to mott & Mallet, 2004; Willmott & Freitas, 2006), they reflect understorey conditions, and cages were may also cause reproductive isolation and thus watered and sprayed multiple times each day so as potentially lead to speciation. to keep humidity levels high. Butterflies were pro- This paper aims to provide new morphological and vided nourishment in the form of sugar water solu- ecological information that will help clarify the taxo- tion (at approximately 20% sugar concentration) in nomic relationships and the reproductive barriers small suspended cups filled with segments of red that occur in this genus, thereby providing insights straws so as to imitate flowers. Commercially avail- on the mechanisms of speciation. We
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