Our response to Heymann & Fuzessy

It was the day before my maternity leave started that I received an invite from the journal Proceedings of the Royal Society B to submit a reply to the comment by Heymann & Fuzessy. They criticized some of the work my co-authors and I published in early 2020, on the relationship between palm fruit colours and the diversity of trichromatic vision (the ability to distinguish red and green) in primates. See here for the original publication. Luckily, the journal allowed me a bit of time to think about a response while nursing my baby.

The main issue that Heymann & Fuzessy raised, was that there is little natural history information on the dependence of primates on palm fruits, especially in Africa. Therefore, they considered the macroecological and macroevolutionary analyses we performed in our original article unreliable. In our response, we argue that our macro analyses, which show a strong relationship between the spatial and temporal diversity of trichromatic primates and that of conspicuous (e.g. reddish) palm fruits (see figure below), are indeed only one piece of the puzzle, and multiple lines of evidence are needed to further resolve the question whether primates evolved trichromatic vision as an adaptation to detect conspicuous fruits. This includes more natural history information – the dataset of Heymann & Fuzessy was limited and incomplete, especially for Africa – , network analyses, co-phylogenetic methods, and macro approaches as we did here, and perform these across a range of taxonomic plant groups that may be important food sources for primates. Good ones to start with could be Moraceae (figs and relatives), Melastomataceae, Annonaceae.

I hope to further address the question on whether palm fruits are important to explain the distribution and diversity of frugivores (including primates) in my future research.

Results from the original study, showing with structural equation models that the proportion of plants with conspicuous fruits in communities have a strong effect on species richness of day-active, frugivorous polymorphic and trichromatic primates in those same places.

Original publication: https://royalsocietypublishing.org/doi/10.1098/rspb.2019.2731

Comment: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.1423

Reply: https://royalsocietypublishing.org/doi/10.1098/rspb.2020.2981

New article: Primate colour vision linked to palm fruit colours

Press release by iDiv (Kati Kietzmann)

Read the open access article here

Data for the article can be downloaded here

Colourful fruits may be the reason why primates can distinguish between shades of red, green and blue

Leipzig/Amsterdam. The evolution of colour vision might be closely linked to the availability of food. Researchers from the German Centre for Integrative Biodiversity Research (iDiv), Leipzig University (UL), and the University of Amsterdam (UvA) found that colour vision in African primate species, which is similar to that of humans, is related to the spatial distribution of palm fruit colours. The results of their study have been published in Proceedings of the Royal Society B. They shed new light on the evolution of primates.

In our retina, three kinds of receptors are responsible for the perception of basic colours: red, green and blue. The same holds true for many primate species – in contrast to all other mammals. For nocturnal species, the ability to distinguish different colours would not provide a significant advantage. It is therefore highly probable that so-called trichromatic vision developed in diurnal primates. In addition to greens and blues, they can also distinguish shades of red, making it easier to detect coloured fruit. This could provide a competitive advantage over other fruit-eating animals that cannot distinguish red from green. While this idea had been tested experimentally in a few species, it remained largely unexplored on a larger scale.

A team of researchers from iDiv, UL and UvA has now shown that trichromatic vision in primates is strongly linked to the availability of conspicuous, red palm fruits. Their research involved analysing data on the colour vision and distribution of more than 400 primate species as well as fruit colour data for over 1700 palm species. The result was clear: trichromatic vision in primates is most common in African countries with a high proportion of palm species with very colourful, conspicuous fruits.

This relationship is a win-win situation, benefiting both primates and palms: while primates rely on palm fruits as their primary food source, they are also important seed dispersers in tropical forests, particularly for large fruits. The research shows that the number of diurnal, fruit-eating primates in Africa increases with the proportion of conspicuous palm fruits, with a peak in subtropical regions. The results suggest that the effects of palm fruits on primates are strongest in the transition zones of arid to subtropical regions, where competition for food is also high. For the African primates, the ability to see several colours is thus an advantage when foraging. Palms, in turn, evolved colourful fruits that could be easily spotted by the primates, thus helping to disperse their seed.

The researchers did not only analyse data from the African continent, but also from Asia and the Americas. “Interestingly, in the Americas and Asia some primate species have trichromatic vision, whereas others do not. Here, we did not identify a relationship between colour vision and the proportion of conspicuous palm fruits,” said first author Dr Renske Onstein from iDiv and UL. Furthermore, most primates in the Americas prefer palm fruits with non-conspicuous colours. By contrast, many trichromatic primates in Asia have no interest whatsoever in a fruit’s colour – they enjoy feeding on large amounts of fruit in general.

“In Asia and the Americas, birds and bats could play a more important role as seed dispersers than primates,” explained Dr Daniel Kissling from UvA, senior author of the study. “In contrast, there are relatively few frugivorous birds on the African continent, so palm species may rely more on primates as seed dispersers than other fruit-eating animals.” The analyses show that palm species in Africa are dominated by those with conspicuous fruits, whereas the fruits of American species tend to be more inconspicuous.

Many primate species are now threatened with extinction due to rapid habitat loss and global changes. This may have cascading effects, especially when some plant species rely on primates as their primary seed dispersers. Thus, conservation efforts should also take plant-animal interactions and fruit-colour diversity into account as this is crucial for maintaining tropical biodiversity.

Original publication

Onstein RE, Vink DN, Veen J, Barratt CD, Flantua SGA, Wich SA, Kissling WD (2020). Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems. Proc. R. Soc. B 20192731. DOI: 10.1098/rspb.2019.2731

http://rspb.royalsocietypublishing.org/lookup/doi/10.1098/rspb.2019.2731

Chimpanzee (Pan troglodytes) feeding on a wild date palm (Phoenix reclinata). (Picture: M. McLennan / Bulindi Chimpanzee & Community Project)

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See you at Evolution in Montpellier?!

From 19-22 August 2018 I will attend the Evolution conference in Montpellier, France. I will present a poster on “Fruit colour as a driver for the evolution of trichromatic primate diversity” in S-33 Ecological models of macroevolution. Please visit me and / or my poster during the ‘Cocktail Poster Session 5.30pm –7.30pm’ on Tuesday 21st, or any other time!

 

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Sneak preview….

The mutualism between fruits and frugivores is prominent in tropical rainforests, but to what extent fruits have influenced the macroevolution and macroecology of frugivores and their functional traits remains underexplored. Here, we hypothesize that trichromatic colour vision (i.e. the ability to distinguish green and red) in frugivorous primates has evolved as an adaptation to detect conspicuously coloured (i.e. reddish) fruits against a background of green foliage. The readily detection of these fruits as critical resources may have provided trichromatic primates a competitive advantage over dichromatic primates that cannot distinguish reds from greens.

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To test this hypothesis, we combined global distribution, phylogenetic and colour vision data for >400 primate species with fruit colour data for >1700 palm and >80 fig species. Palms (Arecaceae) and figs (Ficus) are considered keystone resources for frugivores in tropical rainforests worldwide. We used structural equation modelling to show that the regional proportion of food plant species with conspicuously coloured fruits positively affects the diversity of trichromatic primates, but only in Africa. We show that this effect intensifies towards the tropics, following a hump-shaped relationship with food plant species richness. This suggests that the most species-rich places (i.e. rainforests) provide sufficient alternative food sources for primates, decreasing their dependence on conspicuous fruits. Overall, our results indicate that the consumption of palm and fig fruits could have been a driver for the diversification of trichromatic colour vision in African primates, and that food availability is an important determinant of frugivore diversity more generally.