Evolution of pollination by frugivorous birds in Neotropical Myrtaceae

Abstract

Bird pollination is relatively common in the tropics, and especially in the Americas. In the predominantly Neotropical tribe Myrteae (Myrtaceae), species of two genera, Acca and Myrrhinium, offer fleshy, sugary petals to the consumption of birds that otherwise eat fruits, thus pollinating the plants in an unusual plant-animal interaction. The phylogenetic position of these genera has been problematic, and therefore, so was the understanding of the evolution of this interaction. Here we include new sequences of Myrrhinium atropurpureum in a comprehensive molecular phylogeny based on a balanced sample of two plastid and two nuclear markers, with the aim of providing the historical framework of pollination by frugivorous birds in Myrteae. We developed 13 flower and inflorescence characters that comprehensively depict the macroscopic morphological components of this interaction. Bayesian and parsimony phylogenies concur in placing both Acca and Myrrhinium in a clade with Psidium species; with Myrrhinium sister to Psidium. Mapping of morphological characters indicated some degree of convergence (e.g., fleshy petals, purplish display) but also considerable divergence in key characters that point to rather opposing pollination strategies and also different degrees of specialization in Acca versus Myrrhinium. Pollination by frugivorous birds represents a special case of mutualism that highlights the evolutionary complexities of plant-animal interactions.

Potential pollen vectors of the mass flowering tree Acacia dealbata, within its natural range in southern Tasmania

“…2). Several previously documented cases of bird pollination of nectarless flowers also reported that floral tissues were consumed (Sérsic & Cocucci 1996, Dellinger et al 2014, Nadra et al 2018. We are unable to comment on the relative nutritional value of the floral components and/ or parasitising gall insects, but it is known that two other species of parrot occurring in our study region (Swift Parrot Lathamus discolor and Musk Lorikeet Glossopsitta concinna) intentionally consume and digest the pollen of Eucalyptus (Gartrell & Jones 2001, Hingston et al 2004a.…”

“…A. dealbata is the earliest flowering of all Tasmanian acacias and if outcrossing by insects was of critical evolutionary importance then we might expect that selection pressure on the phenology would have caused a shift to later flowering. The species does not produce nectar from either flowers or extra-floral nectaries and this, together with the yellow flowers and distinctive scent, is inconsistent with traditional bird pollination syndromes which are characterised by the production of abundant nectar to support energetic needs, red colour, and little scent (Faegri & van der Pijl 1979, Nadra et al 2018. However, since some bird species were observed to consistently feed on and among the flowers (table 3) they must clearly be deriving some benefit.…”

The Taming of Psidium guajava: Natural and Cultural History of a Neotropical Fruit

“…The geographic distribution of the complex extends from Mexico to northern Argentina and Uruguay, including the Antilles ( Figure 4 ). A molecular phylogenetic analysis shows P. guajava and P. guineense as sister taxa ( Salywon, 2003 ), but the relationships with the other species are unclear due to lack of representation ( Rivero et al, 2012 ; Nadra et al, 2018 ).…”

“…Phylogenetic studies based on nuclear and plastid DNA regions have confirmed the monophyly of Psidium with Myrrhinium as its sister group (Lucas et al, 2005;Vasconcelos et al, 2017;Nadra et al, 2018;Flickinger et al, 2020). However, evolutionary relationships within the genus remain unresolved due to its high rates of diversification (Vasconcelos et al, 2017), its wide Neotropical distribution (Richardson and Rejmánek, 2011;Landrum, 2017), variable ploidy levels (Costa and Forni-Martins, 2007), and hybridization among species (Landrum et al, 1995).…”