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Beetle pollination of two species of Zamia: Evolutionary and ecological considerations
Abstract
Neither the insects nor the cycads are separately capable of long-term survival in nature, and unless both are protected and conserved, wild populations of Xamia are in jeopardy.
... Much of the Neotropical cycad genus Zamia are pollinated by Rhopalotria weevils and closely related genera within the Allocorynina (Tang et al., 2018). These weevils feed and reproduce on the pollen cone of their host Zamia (Norstog and Fawcett, 1989;Norstog et al., 1992). Conversely, the host Zamia species are completely dependent upon pollination services by the weevils (Norstog et al., 1986;Tang, 1987). ...
... Conversely, the host Zamia species are completely dependent upon pollination services by the weevils (Norstog et al., 1986;Tang, 1987). The Zamia-Rhopalotria symbiosis appears to be fully mutualistic for both lineages, and the relationship has been hypothesized to exhibit phylogenetic congruence between specialized partners (Norstog et al., 1992;Stevenson et al., 1998;Tang et al., 2018). However, studies remain to be done that provide information about potential coevolutionary mechanisms involved, including those documenting reciprocal evolutionary change in each lineage (e.g., Janzen, 1980). ...
... This mutualism is mediated by plant volatile production , a cue that is important for lifecycle completion in both lineages. The strength of the mutualism is such that pollinators go into diapause during the 10 months of the year when reproductive services are not required by the host plant (Norstog and Fawcett, 1989;Norstog et al., 1992). ...
Coevolution between plants and insects is thought to be responsible for generating biodiversity. Extensive research has focused largely on antagonistic herbivorous relationships, but mutualistic pollination systems also likely contribute to diversification. Here we describe an example of chemically-mediated mutualistic species interactions affecting trait evolution and lineage diversification. We show that volatile compounds produced by closely related species of Zamia cycads are more strikingly different from each other than are other phenotypic characters, and that two distantly related pollinating weevil species have specialized responses only to volatiles from their specific host Zamia species. Plant transcriptomes show that approximately a fifth of genes related to volatile production are evolving under positive selection, but we find no differences in the relative proportion of genes under positive selection in different categories. The importance of phenotypic divergence coupled with chemical communication for the maintenance of this obligate mutualism highlights chemical signaling as a key mechanism of coevolution between cycads and their weevil pollinators.
... Exclusion experiments on two of these species indicate that they are pollinators of cycads (Tang 1987;Valencia-Montoya et al. 2017), and it is probable that these ancient plant and beetle lineages have coevolved for many millions of years. Leschen and Buckley (2007) hypothesize that fungivory may be the ancestral state in the Erotylidae, however, adult and early instar larvae of Pharaxonotha floridana (Casey) inhabiting cycad cones appear to be pollen feeders, while late instar larvae feed on cone sporophyll and axis tissue (Norstog et al. 1992). Tang et al. (2018bTang et al. ( , 2020 presented preliminary relationships of species within Pharaxonotha, based on analysis of the 16S rRNA gene, recognizing three distinct radiations: early-diverging lineages, a Caribbean radiation and a recent radiation. ...
... Alternatively, there may have been a number of host-shifts in Pharaxonotha from possibly older, extinct lineages of cycads onto more recently evolved species or onto other genera of cycads (Tang et al. 2018b(Tang et al. , 2020. Unlike other species of Pharaxonotha in Florida, Mesoamerica and Central America which co-inhabit cones with Allocorynina weevils (Tang 1987;Norstog et al. 1992;O'Brien and Tang 2015;Tang et al. 2018aTang et al. , 2018bTang et al. , 2020 in other species of cycads in the genera Ceratozamia, Dioon and Zamia, P. taylori and P. thomasi appear to be the sole cone inhabitants and pollinator of their hosts. ...
Two species of the early-diverging lineages of Pharaxonotha Reitter (Coleoptera: Erotylidae: Pharaxonothinae) are described: Pharaxonotha taylori Skelley and Tang, new species, and Pharaxonotha thomasi Skelley and Tang, new species. A new key to described species of Pharaxonotha, based on previously unused characters, is presented. In recent phylogenetic analyses of beetle diversity based on a large nuclear data set (McKenna et al. 2019) and on nuclear and mitochondrial legacy loci (Powell, pers. comm. 2020), the New World genus Pharaxonotha Reitter (Erotylidae: Pharaxonothinae) was shown to be sister to all remaining Erotylidae in a clade comprised of the Erotylidae+Phytophaga, which includes Cucujoidea, Chrysomeloidea and Curculionoidea. Since these three superfamilies of Coleoptera contain the majority of beetle pest taxa on human plant crops, a closer examination of this genus may provide some insight into the origin and evolution of these insect groups of agricultural concern. Except for the type species of Pharaxonotha, P. kirschii Reitter, which is a minor stored products pest, all other species of the genus that have been studied are inhabitants of cycad cones (Pakaluk 1988; Chaves and Genaro 2005; Franz and Skelley 2008; Skelley and Segalla 2019). Exclusion experiments on two of these species indicate that they are pollinators of cycads (Tang 1987; Valencia-Montoya et al. 2017), and it is probable that these ancient plant and beetle lineages have coevolved for many millions of years. Leschen and Buckley (2007) hypothesize that fungivory may be the ancestral state in the Erotylidae, however, adult and early instar larvae of Pharaxonotha floridana (Casey) inhabiting cycad cones appear to be pollen feeders, while late instar larvae feed on cone sporophyll and axis tissue (Norstog et al. 1992). Tang et al. (2018b, 2020) presented preliminary relationships of species within Pharaxonotha, based on analysis of the 16S rRNA gene, recognizing three distinct radiations: early-diverging lineages, a Caribbean radiation and a recent radiation. Pharaxonotha may inhabit cycad cones in the New World with other beetle genera, including Ceratophila Tang, Skelley and Perez-Farrera (Erotylidae: Pharaxonothinae) in the cycad host Ceratozamia Brongn., and primitive weevils of the subtribe Allocorynina (Belidae) in the host cycads Dioon Lindl. and Zamia L. (O’Brien and Tang 2015; Tang et al. 2018a, 2018b, 2020). The purpose of this paper is to describe two species in the early-diverging lineages of Pharaxonotha identified in those analyses as D0063 from Panama and D0066 from Honduras, inhabiting the cycad genus Zamia. A revised key to all species of Pharaxonotha is presented. Only previously described species of the Caribbean and recent radiations are represented in this review. Others in these and the early-diverging lineages will be described in future papers.
... Ovules are pollinated by Zamia-specialist beetles, Pharaxonota portophylla (Coleoptera: Erotylidae) (Franz & Skelley, 2008). This interaction involves a sequential brood-site reward-deception pollination system, where the plants and the insects are mutually dependent upon one another (Norstog, Fawcett & Vovides, 1992). Beetles exclusively feed on pollen and male cone tissue, probably mate inside the cones, and use them as a brood place (Norstog & Nicholls, 1997). ...
... Beetles exclusively feed on pollen and male cone tissue, probably mate inside the cones, and use them as a brood place (Norstog & Nicholls, 1997). The life span of the insects is unknown, but several generations are produced during the host reproductive season (Norstog, Fawcett & Vovides, 1992;Norstog & Nicholls, 1997). Pollination occurs when receptive female plants produce volatile compounds that mimic male scents and attract pollen-covered insects (Pellmyr et al., 1991;Terry et al., 2004;Proches & Johnson, 2009). ...
Variation in plant reproductive success is affected by ecological conditions including the proximity of potential mates. We address the hypothesis that spatial distribution of sexes affects female reproductive success (RS) in the dioecious cycad, Zamia portoricensis. Are the frequencies of males, operational sex ratios, and distances to the nearest mate associated with RS in females? We studied the spatial distribution of sexes in two populations in Puerto Rico and compared RS of target females with the number of males and operational sex ratios. Population structure suggests regular successful recruitment. Adults, males, and females were randomly distributed with respect to one another. Reproductive success of females was highly variable, but was higher in neighborhoods with more males than females and generally decreased with increasing distance to the nearest male, becoming statistically significant beyond 190 cm. This possible mate-finding Allee effect indicates that pollinator movement among plants may be limited for this mutually dependent plant-pollinator interaction. Yet being close to male plants is a matter of chance, perhaps a factor generating the high intra-population genetic diversity in Z. portoricensis.
... One of these resources is heat produced by flowers (thermogenesis). Thermogenic flowers and inflorescences are present in other botanical families such as Araceae [16][17][18]20,84,91], Arecaceae [21,22], Cyclanthaceae [16,25,92], Magnoliaceae [31,32], and Nymphaeaceae [50], and even in cantharophilous gymnosperms [37]. According to these references, thermogenesis events, in the majority of species from these families, are mostly linked to the period of nocturnal anthesis and the attraction of nocturnal Cyclocephala. ...
The evolutionary trajectories of insects and angiosperms appear to be intimately interconnected. Increases in the diversity of phytophagous beetles and angiosperms co-occur in the Mesozoic fossil record, and there is fossil evidence of pollinivory and pollination by insects, both in flowering plants and in gymnosperms. The oldest records of angiosperm pollination indicate flies as pollen vectors. A basal group of angiosperms, the order Magnoliales, has retained plesiomorphic characters such as dozens of pistils and stamens spiraling around the receptacle. In a family of this order, Annonaceae, over 90% of species are pollinated by beetles. In many Annonaceae species, flowers display wide spaces, referred to as floral chambers, where beetles can find shelter from weather conditions and predators, food in the form of pollen and tissues, and a mating site. Two basic types of floral chambers can be distinguished: small chambers visited by small beetles (Nitidulidae, Staphylinidae, Chrysomelidae, and Curculionidae) with diurnal and/or nocturnal activity and large and thermogenic floral chambers visited by beetles of the tribe Cyclocephalini (Scarabaeoidea, Melolonthidae). In the latter case, the heat that the flowers produce may serve as a resource for the beetles that visit them, resulting in smaller endothermy costs for the scarabs. This study reviewed the literature including PhD and MSc theses on cantharophilous Annonaceae in the Cerrado. In this biome, both types of associations are found, although cantharophilous Annonaceae represent a small portion of the plant species (
... Field surveys in recent decades have identified three major lineages of beetles in the northern hemisphere that have life cycles intricately tied to the male cones of cycads (Tang 1987a;Vovides 1991;Norstog et al. 1992;Oberprieler 1995Oberprieler , 2004Tang et al. 1999;Franz and Skelley 2008). Dissection of adults and/or larvae living in the cones of these cycads indicates that they eat cycad pollen or other cone tissues and may sequester cycad toxins (Norstog and Fawcett 1989;O'Brien and Tang 2015;Xu et al. 2015;Skelley et al. 2017;Tang et al. 2018b). ...
Three groups of beetles inhabit cones of cycads (Cycadales) in the northern hemisphere and are believed to be involved in their pollination. The primitive weevil subtribe Allocorynina (Coleoptera: Belidae) is restricted to the New World cycad genera Dioon Lindl. and Zamia L. One group of weevils (Curculionidae), found only in Cycas L., appears to be a relatively recent colonizer of northern hemisphere cycads. Members of the beetle subfamily Pharaxonothinae (Erotylidae) occur in all Asian and New World cycad genera. Phylogenetic trees of these beetles, based on DNA analysis and supported with morphological studies, are compared to patterns of continental drift and cycad phylogenies. Laurasian origins are suggested for these beetle groups with high latitude dispersal for at least one of these groups during periods of global warm climates.
... In both these examples, the weevil oviposits into microsporophylls of pollen cones, within which the developing larvae feed on starch-rich tissue (Tang 1987b;Norstog & Fawcett 1989). Zamia integrifolia and its beetle pollinator, Pharaxonotha floridana, also fit model A. The adults and early instar larvae of this beetle feed on pollen released by microsporangia (Norstog et al. 1992). Adults of all three of these beetle species, having finished feeding on the deteriorating cone, as well as adults that have emerged from their pupal cases, will leave the vicinity of the depleted pollen cone, usually with their bodies laden with pollen, in search of another pollen cone brood site. ...
Most cycads have intimate associations with their insect pollinators that parallel those of well‐known flowering plants, such as sexually deceptive orchids and the male wasps and bees they deceive. Despite this, the mistaken belief that cycads are mostly wind‐pollinated is still commonly expressed. Perhaps as a consequence, cycad–pollinator systems are rarely exemplified in studies of the role of pollinators in plant evolution and diversification. Although first recognised more than a century ago, specialised associations between cycads and their insect pollinators have been elucidated experimentally only in the past few decades. This review covers the history of understanding pollination in cycads, the advances that have been made since the 1980s using field observations and experiments, and analyses of molecular data from the population to phylum level. We outline areas for future research to address how such interactions might have affected speciation and extinctions. We stress that inclusion of cycads in broader considerations of the role of pollinators in plant diversification is important because they are phylogenetically distant from flowering plants and their pollination systems might have evolved independently of one another. This review is timely because cycads are a globally threatened group that might be vulnerable to co‐extinction with pollinator loss.
... In recent years, several species of pollinators from Asia, Neotropics, and North America have been collected from Cycas (Old World) and Zamia (New World) (Norstog et al. 1986;Tang 1987;Pakaluk 1988;Norstog et al. 1992;Tang et al. 1999). More recently, several species from Asia have been described or assigned to the new genus Cycadophila (Xu et al. 2015;Skelley et al. 2017), or some species of Pharaxonothinae were analyzed using 16S marker (Tang et al. 2018). ...
Two new species of Pharaxonotha Reitter, 1875 are described from Mexico. Illustrations are provided, as a key to identify Pharaxonotha known from the New World. The genus Ceratozamia Brongn (Zamiaceae) is recorded as a host to Pharaxonotha mexicana sp. nov. y P. tenuis sp. nov. for the rst time. Specimens were collected directly in the cones of males and females of C. tenuis.
... In recent years, several species of pollinators from Asia, Neotropics, and North America have been collected from Cycas (Old World) and Zamia (New World) (Norstog et al. 1986;Tang 1987;Pakaluk 1988;Norstog et al. 1992;Tang et al. 1999). More recently, several species from Asia have been described or assigned to the new genus Cycadophila (Xu et al. 2015;Skelley et al. 2017), or some species of Pharaxonothinae were analyzed using 16S marker (Tang et al. 2018). ...
RESUMEN. Dos nuevas especies de Pharaxonotha Reitter, 1875 son descritas desde México. Ilustraciones y una clave para identificar las especies conocidas de Pharaxonotha del Nuevo Mundo son dadas. El género Ceratozamia Brongn (Zamiaceae) se registra como hospedero de Pharaxonotha mexicana sp. nov. y P. tenuis sp. nov. por primera vez. Los especímenes fueron colectados directamente en los conos de machos y hembras de C. tenuis.
ABSTRACT. Two new species of Pharaxonotha Reitter, 1875 are described from Mexico. Illustrations are provided, as a key to identify Pharaxonotha known from the New World. The genus Ceratozamia Brongn (Zamiaceae) is recorded as a host to Pharaxonotha mexicana sp. nov. y P. tenuis sp. nov. for the first time. Specimens were collected directly in the cones of males and females of C. tenuis.
Two major lineages of beetles inhabit cycad cones in the New World: weevils (Curculionoidea) in the subtribe Allocorynina, including the genera Notorhopalotria Tang and O’Brien, Parallocorynus Voss, Protocorynus O’Brien and Tang and Rhopalotria Chevrolat, and beetles in the family Erotylidae, including the genus Pharaxonotha Reitter. Analysis of the 16S ribosomal RNA (rRNA) mitochondrial gene as well as cladistic analysis of morphological characters of the weevils indicate four major radiations, with a probable origin on the cycad genus Dioon Lindl. and comparatively recent host shifts onto Zamia L. Analysis of the 16S rRNA gene for erotylid beetles indicates that an undescribed genus restricted to New World Ceratozamia Brongn. is the most early-diverging clade, and this lineage is sister to a large radiation of the genus Pharaxonotha onto Zamia, with apparent host shifts onto Dioon and Ceratozamia. Analysis of beetles are in accord with current models of continental drift in the Caribbean basin, support some proposed species groupings of cycads, but not others, and suggest that pollinator type may impact population genetic structure in their host cycads.
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