Mating patterns and pollinator mobility are critical traits in forest fragmentation genetics

Abstract

Most woody plants are animal-pollinated, but the global problem of habitat fragmentation is changing the pollination dynamics. Consequently, the genetic diversity and fitness of the progeny of animal-pollinated woody plants sired in fragmented landscapes tend to decline due to shifts in plant-mating patterns (for example, reduced outcrossing rate, pollen diversity). However, the magnitude of this mating-pattern shift should theoretically be a function of pollinator mobility. We first test this hypothesis by exploring the mating patterns of three ecologically divergent eucalypts sampled across a habitat fragmentation gradient in southern Australia. We demonstrate increased selfing and decreased pollen diversity with increased fragmentation for two small-insect-pollinated eucalypts, but no such relationship for the mobile-bird-pollinated eucalypt. In a meta-analysis, we then show that fragmentation generally does increase selfing rates and decrease pollen diversity, and that more mobile pollinators tended to dampen these mating-pattern shifts. Together, our findings support the premise that variation in pollinator form contributes to the diversity of mating-pattern responses to habitat fragmentation.

Figure 1

Map showing regional overview of the six sites where seeds were collected from maternal plants from three eucalypt species across a density gradient caused by habitat fragmentation (a, b). Inset maps (c–g) show intact woodland sites: Scotia Sanctuary (c), Bakara Conservation Park (d), Brookfield Conservation Park (e), Yookamurra Sanctuary (f), Lowan Conservation Park (g). Sampling from the more fragmented Monarto region is shown in inset maps (h–j).

Figure 2

Relationships between mating patterns and density of three mallee eucalypts. Insect-pollinated Eucalyptus gracilis (a) and E. socialis (b) outcrossing rate (t_m, where the selfing rate s=1−t_m) shown by filled squares, biparental inbreeding (t_m−t_s) by filled triangles and correlated paternity (r_p) by filled circles. The bird-pollinated E. incrassata mating patterns are shown by corresponding open shapes (c). The trendlines show slopes (ß) and goodness of fit (r²) of linear regressions between log density and mating patterns. 95% CI are not shown as they fall within the outer edge of each symbol.

Figure 3

Mean effect sizes (Hedges' d*) of habitat fragmentation on animal-pollinated woody plant-mating patterns. Overall mean effect shown in (a) and effects separated by pollinator mobility in (b). Error bars show bias-corrected 95% bootstrap CIs. A mean effect size is significantly different from zero when its 95% CI does not overlap zero. Positive mean effect sizes indicate that the fragmented group of maternal plants had on average larger values for the given mating pattern. The number of studies is shown in parentheses.