Competition drives flower colour evolution in a biodiversity hotspot

The find­ings of a new study pub­lished in Evol­u­tion Let­ters help explain the coex­ist­ence of many closely related flower­ing plant spe­cies, in one of the most diverse tem­per­ate eco­sys­tems in the world. Lead author Dr Alex Skeels tells us more.

Flowers are some of the most beau­ti­ful and fas­cin­at­ing struc­tures in nature and most people can recog­nise a hand­ful of plant spe­cies just from the sight of their flowers (think roses, or Bank­si­as if you’re Aus­trali­an). In fact, most plant spe­cies’ flowers are so unique that they are among the most import­ant fea­tures used by tax­onom­ists and nat­ur­al­ists to identi­fy spe­cies in the field. Angio­sperms, or flower­ing plants, are the most diverse group of plants on the plan­et, and it has long been sus­pec­ted that the huge diversity in flower size, shape, col­our, and scent, may explain this. So, under­stand­ing how flowers evolve over time is key to under­stand­ing the ori­gin of plant biodiversity.

Nat­ur­al selec­tion is the great evol­u­tion­ary force that shapes com­plex struc­tures like flowers, but sev­er­al dif­fer­ent agents of selec­tion may be involved in shap­ing the diversity of flowers. The main role of flowers is to attract pol­lin­at­ors to share pol­len with indi­vidu­als of the same spe­cies. But selec­tion might push flowers of dif­fer­ent pop­u­la­tions of a spe­cies to diverge when, for example, pop­u­la­tions bene­fit from attract­ing dif­fer­ent pol­lin­at­ors in dif­fer­ent eco­lo­gic­al com­munit­ies. This can lead to spe­ci­ation as the diver­ging pop­u­la­tions no longer share pol­len and there­fore no longer repro­duce sexually. 

Pol­lin­at­ors can play an import­ant role in shap­ing the diversity of flowers. Photo from Pixabay https://pixabay.com/photos/hummel-insect-flower-hymenoptera-3609080/

In oth­er cases, indi­vidu­als of dif­fer­ent spe­cies might have sim­il­ar flowers, and would be expec­ted to attract sim­il­ar pol­lin­at­ors. This might not mat­ter too much if there are plenty of pol­lin­at­ors avail­able, if there is not a strong cost to shar­ing pol­len, or those spe­cies do not occur togeth­er in the same com­munit­ies, and flowers might remain the same or change in response to changes in loc­al pol­lin­at­ors over time. But as soon as these con­di­tions change and com­pet­i­tion for pol­lin­at­ors between spe­cies with sim­il­ar flowers increases then we expect nat­ur­al selec­tion to favour divergence.

These examples dif­fer in wheth­er flower diver­gence drives spe­ci­ation, or wheth­er flower diver­gence comes later, either drift­ing in response to loc­al changes in pol­lin­at­or com­munit­ies or driv­en by com­pet­i­tion and oth­er neg­at­ive inter­ac­tions between spe­cies. This is an import­ant dis­tinc­tion in under­stand­ing wheth­er flower diver­gence is a cause or a con­sequence of plant biod­iversity. But how do we tell these scen­ari­os apart? In this study we came up with some pre­dic­tions of what we would expect under these three dif­fer­ent scen­ari­os. We tested these pre­dic­tions in Hakea spe­cies from South­w­est Australia. 

Hakea are a fas­cin­at­ing genus of plants endem­ic to Aus­tralia. They show excep­tion­al diversity in the Medi­ter­ranean-cli­mate region of South­w­est Aus­tralia which is a recog­nised biod­iversity hot­spot due to its high diversity of endem­ic plants under threat from human land-use modi­fic­a­tions, par­tic­u­larly from agri­cul­ture (the region’s known as the wheat-belt). The region is fam­ous for its fairly extreme envir­on­ment (poor soils and hot dry sum­mers) and super-rich plant com­munit­ies, and sit­ting a bit below a sim­il­ar Medi­ter­ranean-type eco­sys­tem, the Cape of South Africa, is one of the most diverse tem­per­ate eco­sys­tems in the world. Hakea are gen­er­ally known as an unfriendly genus of spiky shrubs and per­haps less well recog­nised for their diversity of beau­ti­ful flowers, espe­cially com­pared to their icon­ic rel­at­ives in the Pro­teaceae fam­ily – the Bank­si­as. Pre­vi­ous stud­ies of Hakea by Lamont and col­leagues have shown flower size and col­our to be import­ant traits in determ­in­ing pol­lin­at­or spe­cificity in the genus, so we went about col­lat­ing data and char­ac­ter­ising these traits to test our mod­el predictions.

Flower­ing Hakea spe­cies. Photo: Alex Skeels

To do this, we decided to make use of as much read­ily avail­able data as pos­sible and this meant using digit­al pho­to­graphs to char­ac­ter­ise flower col­our. We used images from the Aus­trali­an Plant Image Index (APII, anbg.gov.au/photo), a resource provided by the Aus­trali­an Nation­al Botan­ic­al Gar­dens in Can­berra (just next to the Aus­trali­an Nation­al Uni­ver­sity where the authors were based), as well as from iNat­ur­al­ist (inaturalist.org) and even Flickr (flickr.com) when no oth­er sources had pho­to­graphs of par­tic­u­lar spe­cies. Our pho­to­graph­ic lib­rary there­fore had a col­lec­tion of pho­tos from pro­fes­sion­al bot­an­ists along­side ama­teur nat­ur­al­ists and cit­izen sci­ent­ists, and rep­res­ents a non-tra­di­tion­al approach to data col­lec­tion that is increas­ingly becom­ing a power­ful resource to sup­port big-data ana­lyses where field-based data col­lec­tion is not always feas­ible. From the pho­tos we could extract val­ues for dif­fer­ent organs in the flower (for example pis­tils and peri­anths, see below) to test our mod­el predictions.

(A) South­west­ern Aus­trali­an flor­ist­ic sur­vey data from Gib­son et al. (2004). (B) Sim­pli­fied illus­tra­tion of the flor­al mor­pho­logy of a Hakea flower, and © inflor­es­cence on stem. Fig­ure taken from paper (https://onlinelibrary.wiley.com/doi/full/10.1002/evl3.225).

We found that Hakea spe­cies typ­ic­ally co-occur with oth­er Hakea spe­cies with very dif­fer­ent flower col­ours, which sug­gests nat­ur­al selec­tion is pre­vent­ing spe­cies with sim­il­ar flowers from co-exist­ing. We also found that, des­pite the genus being over 35 mil­lion years old, flower col­our evolved rap­idly from the Mid-Mio­cene about 15 mil­lion years ago and has sped-up towards the present-day. These pat­terns fit our pre­dic­tions expec­ted from a com­pet­i­tion mod­el of flower evol­u­tion rather than a spe­ci­ation mod­el. This makes sense because in South­w­est Aus­tralia many closely-related spe­cies are packed into com­munit­ies and we expect com­pet­i­tion to be rampant and a strong select­ive force. Yet this res­ult also in some ways goes against the tra­di­tion­al view that flower diver­gence is most import­ant dur­ing spe­ci­ation and while this might be true in many cases, we found that, at least for flower col­our, diver­gence seems to come sub­sequent to spe­ci­ation, as biod­iversity and the num­ber of poten­tial spe­cies inter­ac­tions accu­mu­lated in South­w­est Aus­tralia. Alto­geth­er, the inter­est­ing his­tory of flower evol­u­tion in Hakea helps shine a light on the pro­cesses driv­ing the incred­ible diversity of flowers and flower­ing plants. 

Dr Alex Skeels is cur­rently a post-doc at ETH Zürich and the Swiss Fed­er­al Research Insti­tute for Forest, Snow and Land­scape (WSL). The above work was car­ried out as part of Alex’s PhD with the Mac­ro­e­volu­tion and Mac­roe­co­logy Group from the Aus­trali­an Nation­al Uni­ver­sity and Beha­vi­our­al Eco­logy and Mac­ro­e­volu­tion Group from the Uni­ver­sity of Mel­bourne. The ori­gin­al study is freely avail­able to read and down­load from Evol­u­tion Letters.