Paternity analysis reveals wide pollen dispersal and high multiple paternity in a small isolated population of the bird-pollinated Eucalyptus caesia (Myrtaceae)

Abstract

Optimal foraging behaviour by nectavores is expected to result in a leptokurtic pollen dispersal distribution and predominantly near-neighbour mating. However, complex social interactions among nectarivorous birds may result in different mating patterns to those typically observed in insect-pollinated plants. Mating system, realised pollen dispersal and spatial genetic structure were examined in the bird-pollinated Eucalyptus caesia, a species characterised by small, geographically disjunct populations. Nine microsatellite markers were used to genotype an entire adult stand and 181 seeds from 28 capsules collected from 6 trees. Mating system analysis using MLTR revealed moderate to high outcrossing (t m = 0.479-0.806) and low estimates of correlated paternity (r p = 0.136 ± s.e. 0.048). Paternity analysis revealed high outcrossing rates (mean = 0.72) and high multiple paternity, with 64 different sires identified for 181 seeds. There was a significant negative relationship between the frequency of outcross mating and distance between mating pairs. Realised mating events were more frequent than expected with random mating for plants o40 m apart. The overall distribution of pollen dispersal distances was platykurtic. Despite extensive pollen dispersal within the stand, three genetic clusters were detected by STRUCTURE analysis. These genetic clusters were strongly differentiated yet geographically interspersed, hypothesised to be a consequence of rare recruitment events coupled with extreme longevity. We suggest that extensive polyandry and pollen dispersal is a consequence of pollination by highly mobile honeyeaters and may buffer E. caesia against the loss of genetic diversity predicted for small and genetically isolated populations.

Conservation of old individual trees and small populations is integral to maintain species' genetic diversity of a historically fragmented woody perennial

“…Each of the six relatively large populations of E. caesia analysed was characterized by strong population substructuring and significant positive spatial autocorrelation, supporting predictions of limited seed dispersal and observations of restricted mating (Bezemer, 2018;Bezemer et al, 2016). Similarly high levels of within-population spatial genetic structure are reported for bromeliads restricted to inselbergs in the Brazilian Atlantic rainforest (Barbará et al, 2008).…”

“…Boyagin was previously shown to display a unique pattern of population substructuring, where three genetically differentiated clusters were geographically interspersed (Bezemer et al, ). Recent recruitment from seed is absent in most populations of E. caesia (Bezemer, ; Yates et al, ).…”

“…Population spatial genetic structure was explored for five of the largest sampled stands-Mt Caroline, Mordetta Road, Old Muntadgin, Pingaring and Chiddarcooping. Population spatial genetic structure at Boyagin is reported in a previous study (Bezemer et al, 2016). To test whether genetic substructuring reflects geographic structure within populations, structure analyses assuming an admixture model were performed.…”

“…Geographically isolated populations may still be connected via gene flow mediated by strong‐flying pollinators (Gonçalves‐Oliveira et al, ; Hopper, ), especially in contemporary landscapes where genetic interconnection may be facilitated by the occurrence of introduced or translocated (stepping‐stone) populations in the intervening landscape (Gevaert, Mandel, Burke, & Donovan, ). Nonetheless, some outcrop endemic plants that are pollinated by highly mobile nectar feeding birds show pollen movement that is restricted to within stands or between neighbouring populations (Bezemer, Krauss, Phillips, Roberts, & Hopper, ; Nistelberger et al, ). Further investigation is required to improve understanding of the paradox of strong genetic differentiation despite pollination systems that are predicted to facilitate genetic connectivity among isolated populations (Breed et al, ; Hopper, ).…”

“…Eucalyptus caesia Benth., a long‐lived bird‐pollinated lignotuberous tree endemic on granite outcrops, is a well‐suited species to study patterns of genetic structure and connectivity of historically fragmented populations at a landscape scale (Bezemer et al, ; Byrne & Hopper, ; Moran & Hopper, ). Our study is located in the Southwest Australian Floristic Region (Hopper & Gioia, ), a global biodiversity hot spot with numerous examples of old, climatically buffered infertile landscapes (OCBILs) and, consequently, old plant lineages with complex evolutionary histories (Hopper, ; Hopper, Silveira, & Fiedler, ).…”