Department of Environment and Genetics and the Research Centre for Future Landscapes, La Trobe University, Melbourne, Victoria 3086, Australia.
Ecology and Evolution, Research School of Biology, The Australian National University, Canberra, ACT 2600, Australia.
Ann Bot. 2024 Apr 10;133(2):273-286. doi: 10.1093/aob/mcad178.
Understanding the origin of pollination by sexual deception has proven challenging, as sexually deceptive flowers are often highly modified, making it hard to resolve how any intermediate forms between sexual deception and an ancestral strategy might have functioned. Here, we report the discovery in Caladenia (Orchidaceae) of sexual attraction with pollination during feeding behaviour, which may offer important clues for understanding shifts in pollination strategy.
For Caladenia robinsonii, we observed the behaviour of its male wasp pollinator, Phymatothynnus aff. nitidus (Thynnidae), determined the site of release of the sexual attractant, and experimentally evaluated if the position of the attractant influences rates of attempted copulation and feeding behaviour. We applied GC-MS to test for surface sugar on the labellum. To establish if this pollination strategy is widespread in Caladenia, we conducted similar observations and experiments for four other Caladenia species.
In C. robinsonii, long-range sexual attraction of the pollinator is via semiochemicals emitted from the glandular sepal tips. Of the wasps landing on the flower, 57 % attempted copulation with the sepal tips, while 27 % attempted to feed from the base of the labellum, the behaviour associated with pollen transfer. A similar proportion of wasps exhibited feeding behaviour when the site of odour release was manipulated. A comparable pollination strategy occurs in another phylogenetically distinct clade of Caladenia.
We document a previously overlooked type of sexual deception for orchids involving long-distance sexual attraction, but with pollination occurring during feeding behaviour at the labellum. We show this type of sexual deception operates in other Caladenia species and predict that it is widespread across the genus. Our findings may offer clues about how an intermediate transitional strategy from a food-rewarding or food-deceptive ancestor operated during the evolution of sexual deception.
理解性欺骗授粉的起源具有挑战性，因为性欺骗花通常经过高度修饰，很难确定性欺骗和祖先策略之间的任何中间形式的功能如何。在这里，我们报告了在 Caladenia（兰科）中发现的在取食行为期间进行授粉的性吸引，这可能为理解授粉策略的转变提供重要线索。
对于 Caladenia robinsonii，我们观察了其雄性黄蜂传粉者 Phymatothynnus aff. nitidus（Thynnidae）的行为，确定了性引诱剂释放的位置，并通过实验评估了引诱剂位置是否会影响交配和取食行为的尝试率。我们应用 GC-MS 测试了唇瓣上的表面糖。为了确定这种授粉策略是否在 Caladenia 中广泛存在，我们对另外四个 Caladenia 物种进行了类似的观察和实验。
在 C. robinsonii 中，传粉者的远程性吸引是通过从腺体萼片尖端释放的半化学物质实现的。在落在花朵上的黄蜂中，有 57%的黄蜂试图与萼片尖端交配，而 27%的黄蜂试图从唇瓣底部取食，这种行为与花粉转移有关。当改变气味释放位置时，也有类似比例的黄蜂表现出取食行为。在另一个在系统发育上不同的 Caladenia 分支中也发生了类似的授粉策略。
我们记录了一种以前被忽视的兰花性欺骗类型，涉及远距离性吸引，但授粉发生在唇瓣的取食行为中。我们表明，这种类型的性欺骗在其他 Caladenia 物种中存在，并预测它在属中广泛存在。我们的发现可能提供了关于从中间过渡策略到食物奖励或食物欺骗祖先在性欺骗进化过程中是如何运作的线索。
