T HE LATITUDINAL DIVERSITY GRADIENT OF THE GLOBAL REEF FISH FAUNA IN

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THE LIGHT OF PROCESS

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Théo Gaboriau1, Camille Albouy2, Patrice Descombes3,4,5, David Mouillot1, Loïc Pellissier4,5* Fabien 4

Leprieur1,6*, 5

1. UMR MARBEC, (CNRS, IRD, IFREMER, UM), cc093, Place E. Bataillon, FR-34095 Montpellier, 6

France. 7

2. IFREMER, unité Ecologie et Modèles pour l’Halieutique, rue de l’Ile d’Yeu, BP21105, 44311 8

Nantes cedex 3, France. 9

3. University of Fribourg, Unit of Ecology & Evolution, Ch. du Musée 10, CH-1700 Fribourg, 10

Switzerland. 11

4. Swiss Federal Research Institute WSL, CH-8903 Birmensdorf, Switzerland. 12

5. Landscape Ecology, Institute of Terrestrial Ecosystems, ETH Zürich, 8044 Zürich, Switzerland. 13

6. Institut Universitaire de France, Paris, France 14

* Shared senior authorship. 15 16 17 18 19 20

In preparation for Ecology Letters

2 Numerous historical and ecological hypotheses have been proposed to explain the formation of the 23

Latitudinal Diversity Gradient (LDG). These hypotheses are directly related to the increase of species 24

richness towards the tropics, which ultimately arises through the processes of speciation, extinction 25

and dispersal. However, a mechanistic understanding of the role of these processes in shaping the 26

LDG is currently lacking since most of previous studies used a correlative approach. In this paper, we 27

developed a serie of mechanistic models of diversification driven by habitat changes through 28

geological time to evaluate the predictions of four major hypotheses proposed to explain the LDG, 29

namely the ‘geographic area, ‘tropical niche conservatism’, ‘ecological limits’ and ‘evolutionary 30

speed’ hypotheses. We then compared observed patterns of biodiversity in the global reef fish fauna to 31

those simulated by the mechanistic models. We show that the dual effect of time and habitat area can 32

explain higher species richness in the tropics but do not predict a steep decline of biodiversity towards 33

the temperate climate. Our results suggest that the relative role of the considered hypotheses is nested 34

through time. Habitat changes caused by plate tectonics have shaped the general repartition of reef fish 35

diversity over deep geological time periods, while the expansion of harsher environmental conditions 36

at higher latitudes since the Pliocene have likely produced the marked latitudinal gradient of diversity 37

that we observe today. Overall, this study calls for an increasing use of mechanistic models in the 38

fields of biogeography and macroecology in order to provide a temporal and spatial understanding of 39

the role of speciation, extinction and dispersal in generating contemporary patterns of biodiversity. 40

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The global increase of species diversity towards the equator, commonly referred as the latitudinal 43

diversity gradient (LDG), is the one of the most striking biodiversity patterns on earth. The LDG has 44

been described for most taxonomic groups, at different spatial scales and periods of time (e.g. 45

Hillebrand 2004; Kinlock et al. 2017). 46

Numerous ecological and historical hypotheses have been proposed and debated to explain why 47

species diversity is higher under the tropics (Pianka 1966; Willig et al. 2003; Mittelbach et al. 2007, 48

Brown 2014; Fine 2015). Among them, four major hypotheses are still into thorough scrutiny 49

(reviewed in Fine 2015, see also Table 1). First, the ‘geographic area’ hypothesis posits that tropical 50

regions that covered larger areas over geological time periods support higher population size in 51

average due to larger species ranges, which in turn increases the chances to speciation and decreases 52

the chances of extinction (Rosenzweig 1995; Kisel et al. 2011, Fine & Jetz 2012). Second, the 53

‘tropical niche conservatism’ hypothesis posits that species that tend to specialize to a certain range of 54

temperature or a certain resource, will not survive to important changes, but will outcompete non- 55

specialized species in a stable environment (Janzen 1967; Wiens et al. 2010). Thus, the more stable 56

tropical climates are expected to promote species specialization, which limits their dispersion toward 57

non-optimal temperate regions (Mannion et al. 2014; Cavender-Bares et al. 2011). Third, the 58

‘ecological limits’ hypothesis posits that the total resource availability constrains the number of 59

species that can co-occur in a region (Hutchinson 1959; MacArthur 1965) with a dynamic equilibrium 60

between speciation, dispersion and extinction (Rabosky and Hurlbert 2015). The addition of a new 61

species in a region with fully exploited resources, reduces the average population size, which increases 62

the probability of extinction and decreases the probability of speciation of all present species. Finally, 63

the ‘evolutionary speed’ hypothesis posits that mutation and speciation rates depend on metabolic 64

rates that are correlated with temperature (Allen et al. 2002). Therefore, regions with a warmer climate 65

would support higher speciation rates. Even though those four hypotheses are both widely accepted 66

and not mutually exclusive (Brown 2014), there is still no consensus about the exact role of speciation, 67

extinction and dispersal process in generating and maintaining the LDG. Indeed, these hypotheses 68

4 unexplored.

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To evaluate these hypotheses, previous empirical studies employed either a correlative approach based 71

on curve fitting methods (e.g. Belmaker & Jetz 2015), a macroevolutionary approach based on dated 72

phylogenies and fossils (e.g. Jablonski et al. 2006; Rolland et al. 2014; Siqueira et al. 2016) or a 73

combination of both approaches (e.g. Buckley et al. 2010). Correlative analyses provided important 74

information about the most important factors explaining the global variation of species richness along 75

spatial gradients (e.g. Sandel and Dangremond 2012; Pellissier et al. 2014; Belmaker and Jetz 2015). 76

For instance, Belmaker & Jetz (2015) provided support for the ‘geographic area’ hypothesis by finding 77

a strong statistical relationship between species richness of birds and mammals within the world’s 78

bioregions and their areal extent over 55 million years. However, correlation does not equate to 79

causation and these studies were not able to provide a mechanistic understanding of the role of 80

speciation, extinction and dispersal processes in shaping large-scale patterns of species diversity (see 81

Gavin et al. 2017). 82

To overcome the limitations of correlative approaches, macroevolutionary models based on dated 83

phylogenies or fossils have been used to compare speciation, extinction and dispersal rates between 84

tropical vs. temperate regions (Jablonski et al. 2006; Pyron and Wiens 2013; Rolland et al. 2014; 85

Siqueira et al. 2016). For instance, Rolland et al. (2014) used the Geographic State Speciation and 86

Extinction model (GeoSSE, Goldberg et al., 2011) to test for differences in speciation, extinction and 87

dispersal rates between tropical vs. temperate regions for the world’s terrestrial mammals. Using this 88

approach, Rolland et al. (2014) found higher dispersal rates from the tropics to the temperate regions, 89

hence supporting the ‘tropical niche conservatism’ hypothesis. While these studies improved our 90

understanding of the role of macroevolutionary processes in shaping the LDG, they also showed a 91

number of limitations. First, the GEOSSE approach only considers two regions (e.g. temperate vs. 92

tropical regions), which does not allow a spatial understanding of how speciation, extinction and 93

dispersal have shaped species diversity along the latitudinal gradient. Then, the GEOSSE model does 94

not explicitly integrate the influence of past environmental changes on clade diversification and 95

5 dispersal, which make the inferences with such an approach limited if the objective of the study is to 96

evaluate the role of historical factors (e.g. plate tectonics, early Eocene climate warming, Quaternary 97

glaciations). 98

In this study, we propose a process-based modelling approach (see Rangel et al. 2007; Gotelli et al. 99

2009; Leprieur et al. 2016; Gavin et al. 2017; Connolly et al. 2017; Descombes et al. 2017) to the 100

study of the LDG. Compared to correlative and macroevolutionary approaches, the use of process- 101

based models allows explicitly considering the influence of speciation, extinction and dispersal 102

processes on spatial patterns of species diversity (Rangel et al. 2007, Leprieur et al. 2016). Simulated 103

and observed patterns of species diversity can then be compared under diverse hypotheses (see Rangel 104

et al. 2007; Leprieur et al. 2016). More importantly, process-based models allow one to assess the 105

impact of a particular factor in isolation by holding others factors constant (Rangel et al. 2007), which 106

is particularly needed when testing multiple hypotheses in ecology and biogeography. 107

Recently, Leprieur et al. (2016) proposed a neutral process-based model of diversification, namely the 108

spatial diversification model of lineages through time (SPLIT), which consists in simulating the 109

evolutionary dynamics of species ranges by spatially linking speciation, extinction and dispersal 110

processes to habitat changes over geological time periods. The SPLIT model provides inferences on 111

species range dynamics, species diversity together with the expected rates of speciation and extinction 112

through time. Using this model, Leprieur et al. (2016) showed that plate tectonics played a major role 113

in shaping past and contemporary patterns of tropical reef biodiversity. In this study, we extend the 114

SPLIT model to the study of the LDG in the global reef fish fauna, focusing on spiny-rayed fishes (i.e. 115

Acantomorpha) that are the dominant group of vertebrates, with thousands of species present in all 116

trophic levels of marine networks (Dunne et al. 2004). Specifically, we simulated the evolutionary 117

dynamics of species ranges according to the four above-mentioned hypotheses (i.e. the ‘geographic 118

area’, ‘tropical niche conservatism’, ‘ecological limits’ and ‘evolutionary speed’ hypotheses; see Table 119

1) in order to evaluate their relative influence in shaping the LDG in the global reef fish fauna. 120

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