Diversification and coevolution in brood pollination mutualisms: Windows into the role of biotic interactions in generating biological diversity

Abstract

Brood pollination mutualisms—interactions in which specialized insects are both the pollinators (as adults) and seed predators (as larvae) of their host plants—have been influential study systems for coevolutionary biology. These mutualisms include those between figs and fig wasps, yuccas and yucca moths, leafflowers and leafflower moths, globeflowers and globeflower flies, Silene plants and Hadena and Perizoma moths, saxifrages and Greya moths, and senita cacti and senita moths. The high reciprocal diversity and species-specificity of some of these mutualisms have been cited as evidence that coevolution between plants and pollinators drives their mutual diversification. However, the mechanisms by which these mutualisms diversify have received less attention. In this paper, we review key hypotheses about how these mutualisms diversify and what role coevolution between plants and pollinators may play in this process. We find that most species-rich brood pollination mutualisms show significant phylogenetic congruence at high taxonomic scales, but there is limited evidence for the processes of both cospeciation and duplication, and there are no unambiguous examples known of strict-sense contemporaneous cospeciation. Allopatric speciation appears important across multiple systems, particularly in the insects. Host-shifts appear to be common, and widespread host-shifts by pollinators may displace other pollinator lineages. There is relatively little evidence for a ”coevolution through cospeciation” model or that coevolution promotes speciation in these systems. Although we have made great progress in understanding the mechanisms by which brood pollination mutualisms diversify, many opportunities remain to use these intriguing symbioses to understand the role of biotic interactions in generating biological diversity.

Sex differences in pollinator behavior: Patterns across species and consequences for the mutualism

“…These flowers therefore primarily attract female flies, though males do occasionally visit looking for mates (Renner, 2006). In most of these bee species, males do not visit linators of plants whose developing fruits they use as larval hosts (Hembry and Althoff 2016;Kato & Kawakita, 2017). In most of these bee species, males do not visit linators of plants whose developing fruits they use as larval hosts (Hembry and Althoff 2016;Kato & Kawakita, 2017).…”

A Novel, Enigmatic Basal Leafflower Moth Lineage Pollinating a Derived Leafflower Host Illustrates the Dynamics of Host Shifts, Partner Replacement, and Apparent Coadaptation in Intimate Mutualisms

“…Examples include pollinating seed-predation, ant-myrmecophyte, and leafcutter ant-fungus interactions (Currie et al 2003; Kawakita and Kato 2009; Althoff et al 2012; Cruaud et al 2012 b ; Chomicki et al 2015). In these eukaryotic mutualisms, evidence for strict cospeciation is limited (Cruaud et al 2012 a ; Hembry and Althoff 2016; but see Yang et al 2015), and at some scales in some interactions, phylogenetic congruence is even lacking (e.g., Quek et al 2004; Hembry et al 2013). However, the evidence for both cophylogenetic structure and phylogenetic conservatism across different intimate mutualisms is striking, given the obvious potential for (and clear evidence of) horizontal transfer.…”

Pollinator Diversity: Distribution, Ecological Function, and Conservation

“…These are thought to include some mutually dependent brood site pollination systems such as between some figs and fig wasps, leafflowers and leafflower moths, and yuccas and yucca moths that have evolved from seed parasite relationships, though not all of these relationships are mutually exclusive (Hembry and Althoff 2016). Others are also not mutually dependent where they involve deception of insects that would not normally visit flowers, such as the relationship between Ceropegia spp.…”