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The evolution of latitudinal range limits in tropical reef fishes: heritability, limits, and inverse Rapoport’s rule

Marcio R. Pie, Raquel Divieso, Fernanda S. Caron, Alexandre C. Siqueira, Diego R. Barneche, Osmar J. Luiz
doi: https://doi.org/10.1101/2020.11.02.365700

ABSTRACT

Aim In this study we explore patterns and evolutionary processes of tropical reef fish latitudinal ranges, namely the degree of similarity in range size between ancestor and descendant lineages (i.e. phylogenetic signal); the evolution of range limits; and the latitudinal distribution of range sizes, particularly with respect to Rapoport’s rule.

Location Global.

Taxon Tropical reef fishes.

Methods We integrate data on the latitudinal distribution and evolutionary history of 5,071 tropical reef fish species with phylogenetic comparative methods to assess the level of phylogenetic signal in latitudinal range size, low- and high-latitude limits, and range medians, and to estimate rates of evolution of those traits. Finally, we test whether latitudinal ranges become smaller near the equator, as predicted by Rapoport’s rule, using phylogenetic generalized least squares.

Results There were varying levels of phylogenetic signal in latitudinal range size, low- and high-latitude limits, and range medians. Despite these differences, latitudinal medians were consistently shown to have the highest phylogenetic signal among all measured geographic features. Interestingly, the position of high-latitude limits in general evolved at substantially faster rates than their low-latitude counterparts. Finally, we confirm for the first time the existence of an inverse Rapoport’s rule in marine fishes using phylogenetic comparative methods.

Main conclusions We uncovered several congruent patterns in latitudinal ranges of tropical reef fish, despite vastly disparate biogeographical distributions and ecological differences between the studied fish lineages. Such broad congruence suggests that the evolution of latitudinal ranges of reef fishes may be governed by common principles.

INTRODUCTION

Some of the most pervasive patterns in the distribution of life on earth, such as the latitudinal gradient in species diversity (Willig, Kaufman & Steven, 2003; Hillebrand, 2004; Mittelbach et al., 2007) and the differences in faunal composition between regions (Ficetola, Mazel & Thuiller, 2017; Cowman et al., 2017), are fundamentally determined by the evolution of the position and limits of geographical ranges of different organisms. For instance, phylogenetic niche conservatism posits that the ancestral niche can determine the regions and habitats that a clade can colonize, and those in which it will persist in the face of environmental change (Wiens & Donoghue, 2004). Therefore, understanding the evolution of geographical ranges has far implications for many areas in ecology, conservation and evolution, from biogeography to the response of species to climate change. In this study we focus on three fundamental properties of geographical distributions: the degree of similarity in latitudinal range size between ancestor and descendant lineages, the evolution of range limits, and the geographical distribution of range sizes using tropical reef fishes as a model system. Tropical reef fishes are an ideal group for studying patterns and processes in range size in the marine realm. They are conspicuous members of shallow coral reef ecosystems, facilitating the surveys that provide presence-absence data needed to quantify range sizes. Furthermore, reef fishes are among the most diverse groups of vertebrates in the world, exhibiting extraordinary taxonomic breadth and endemism, with many closely related species that vary greatly in both their range size and in many of the potential biological traits that may influence range size (Ruttenberg & Lester, 2015).

The seminal paper of Jablonski (1987) demonstrated that sister species of Cretaceous mollusks exhibited correlation in their range sizes, thus suggesting that there may be heritability in this emergent trait. However, the generality of species-level “heritability” of emergent traits in general, and of geographical range size in particular, is still unclear. For example, although studies on terrestrial taxa have shown mixed support for range size heritability (e.g. Ricklefs & Latham, 1992; Blackburn & Gaston, 1996; Waldron, 2007), some inferences might have been biased by the low statistical power of the early methods used to test for species level heritability (more recently referred to as phylogenetic signal, see Revell, Harmon & Collaret, 2008), such as variance partitioning. On the other hand, even though model-based methods were more successful in detecting phylogenetic signal in range size (Cardillo, 2015; Pie & Meyer, 2017), they also found substantial differences among lineages depending on their biological characteristics (e.g. Freckleton, Harvey & Pagel, 2002, see also Ricklefs & Latham, 1992). Interestingly, although the original study of Jablonski (1987) involved marine mollusks, no study to date tested for range size heritability in extant marine taxa.

One cannot understand the evolution of geographical range size without first recognizing what determines its limits (Gaston, 2009; Sexton et al., 2009). This issue was well presented by Merriam (1894): “What naturalists wish to know is not how species are dispersed, but how they are checked in their efforts to overrun the earth”. The study of range limits is particularly intriguing in the ocean, given that there are few hard biogeographical barriers that inhibit species dispersal when compared with terrestrial habitats (Palumbi, 1994, but see Gaines et al., 2009). Within marine habitats, the proximate mechanisms driving the distribution of species might involve some combination of environmental tolerances (Rezende & Bozinovic, 2019; Deutsch, Penn & Seibel, 2020; Marshall et al., 2020), species-level traits that have the potential to impact species’ distributions by influencing colonization ability and/or post-colonization survival or persistence (Luiz et al., 2013), and the impact of ocean currents on larval dispersal (e.g. Gaylord & Gaines, 2000; Mora & Sale, 2002; Álvarez-Noriega et al., 2020). While these proximate mechanisms have been scrutinized in the macroecological literature, the ultimate (evolutionary) mechanisms driving range limit evolution in marine species are still poorly known. In terrestrial organisms, tolerance to heat is largely conserved across lineages, whereas tolerance to cold varies between and within species, a pattern that was interpreted as evidence for hard physiological boundaries constraining the evolution of tolerances to high temperatures (Araújo et al., 2013, see also Qu & Wiens, 2020). Indirect evidence of environmental tolerances can be obtained by recording the minimum and maximum latitudes of occurrence of a given species, given the widespread association between geographical distributions and physiological processes, particularly in marine fish (Stuart-Smith et al., 2015; Stuart-Smith, Edgar & Bates, 2017; Waldock et al., 2019; Dahlke et al., 2020). Given that many climatic variables vary consistently with latitude, such limits can serve as a proxy for the corresponding environmental limits. Indeed, Pie & Meyer (2017) found that, for terrestrial vertebrates, rates of evolution of high-latitude limits were 1.6-4 times faster than low-latitude limits, suggesting that different mechanisms drive the evolution of “warm” and “cold” range boundaries. The extent to which this pattern is shared with marine organisms is currently unknown.

Rapoport’s rule states that species that are characteristic of high-latitude locations have greater latitudinal range than species which inhabit low-latitude locations (Rapoport, 1982), and it therefore could provide a mechanism to explain the latitudinal gradient in species richness (Stevens, 1989). Although evidence for Rapoport’s rule has been obtained for several terrestrial taxa, its generality has been called into question (Gaston, Blackburn & Spicer, 1998). Moreover, it has rarely been assessed in marine organisms. For instance, the few studies to date testing Rapoport’s rule for marine fishes found that, not only the rule did not apply, but also that ranges actually became larger towards the equator (Rohde, Heap & Heap, 1993; Macpherson & Duarte, 1994; Macpherson, Hastings & Robertson, 2009, but see Fortes & Absalão, 2010). However, it is important to note that, given the often significant phylogenetic signal in geographical ranges (e.g. Cardillo, 2015; Pie & Meyer, 2017), it is possible that the obtained results might have been affected by phylogenetic nonindependence between species, potentially biasing both the direction and the significance of the estimated relationships. To the best of our knowledge, no study to date tested for the existence of Rapoport’s rule in marine fishes using phylogenetic comparative methods.

In this study we provide a comprehensive assessment of the evolution of geographical ranges in marine reef fishes. In particular, we focus on three main questions: (1) is there significant phylogenetic signal in their latitudinal range sizes? (2) do low- and high-latitude range limits evolve at different rates during their evolution? and (3) do patterns of reef fish latitudinal range size variability support Rapoport’s rule?

MATERIALS AND METHODS

Data collection

Latitudinal limits were obtained from the presence-absence dataset of Rabosky et al. (2018). This dataset consists of global occurrences of marine species in geographic grid cells of 150 km2, and it was built through the AquaMaps algorithm (Ready et al., 2010). From this dataset, we first filtered species that are considered reef-associated (see Siqueira et al., 2020), to then calculate the highest, lowest and median latitudinal points of the geographic distribution of each species. Our final dataset contained distribution data for 5,071 species of tropical reef fishes. We also used the phylogenetic trees produced by Siqueira et al. (2020) to perform our comparative analyses. This set of 100 phylogenies was produced by the taxonomic imputation of missing species into the backbone tree of Rabosky et al. (2018) using the TACT algorithm (Chang, Rabosky & Alfaro, 2020).

Analyses

We estimated the phylogenetic signal of the latitudinal median, as well as the high- and low-latitude limits of tropical reef fishes using Pagel’s λ (Pagel, 1999) and Blomberg et al.’s K (2003) using the phylosig function in PHYTOOLS 0.7-47 (Revell, 2012). More specifically, we tested whether a model with an estimated λ provides a better fit than a simpler alternative where λ=0, whereas K estimates were based on 1,000 resamplings of the original data. Latitudinal range size data were ln-transformed prior to the analyses. We used phylogenetic generalized least squares (PGLS, Freckleton et al., 2002) to test the relationship between the latitudinal range (difference between high and low latitude limits as the response variable) and latitudinal position (predictor variable) using the pgls function in CAPER 1.0.1 (Orme et al., 2008). We estimated the rate of evolution of each geographic feature based on the σ2 parameter under a Brownian Motion (BM) model using the fitContinuous function in GEIGER 2.0.7 (Harmon et al., 2008). Differences in rates of evolution of low- and high-latitude limits were tested using the mvBM function in mvMORPH 1.1.3 (Clavel, Escarguel & Merceron, 2015). This test contrasts the fit of a model in which low- and high-latitude limits share the same rates against an alternative where each limit has a separate rate using likelihood ratio tests. To account for phylogenetic uncertainty, we repeated all analyses on each of the 100 alternative topologies and report the median of the estimates of each parameter and model likelihood. However, given that the phylogenetic imputation used to provide those topologies might have introduced noise in the inferred parameters, we repeated all analyses using a smaller phylogeny (2,585 tips) that included only those species for which genetic data were available. We refer to these datasets as expanded and reduced, respectively. The random imputation of species based on taxonomy can also bias the inferred evolutionary signal of distribution features. Therefore the tests of phylogenetic signal were performed using the reduced dataset only. In each of the above mentioned analyses, we pruned the trees to estimate separately the evolutionary rates and phylogenetic signal for different families and orders, as long as the resulting subtrees had at least 20 tips. All analyses were carried out in R 4.0.2 (R Core Team, 2020).

RESULTS

The distribution of latitudinal ranges in the studied tropical reef fish species follows the typical pattern found in terrestrial organisms, with an approximately lognormal distribution with a left skew (Figure 1). The truncation on the right-hand side of the distribution is probably the result of a geometric constraint in terms of the size of ocean basins, given that the largest possible range (i.e. the natural logarithm of the difference between the maximum and minimum latitudes across all studied species) would be ≈ 4.7. Despite this hard boundary condition, the latitudinal ranges of studied lineages on average tended to be relatively broad, with many species approaching the largest latitudinal range classes. There were varying levels of phylogenetic signal in latitudinal range size, low- and high-latitude limits and range medians, both at the order (Figure 2) and the family levels (Figure S1). Despite these differences, range medians consistently showed the highest levels of phylogenetic signal, both for Pagel’s λ and Blomberg et al.’s K (Tables S1, S2).

Figure 1.
Figure 1.

Distribution of log-transformed latitudinal ranges of the seven most species-rich marine fish orders in our dataset. The largest possible range (i.e. the natural logarithm of the difference between the maximum and minimum latitudes across all studied species) would be ≈ 4.7.

Figure 2.
Figure 2.

Phylogenetic signal, according to Pagel’s λ (Pagel 1999), of properties of geographical ranges of tropical reef fish orders. Details on estimates, corresponding likelihoods and p-values are indicated in Table S1.

Results of statistical tests for variation in rates of evolution between high- and low-latitude limits for different fish orders are shown in Table 1. Significant rate differences were detected in 17 and 13 out of the 19 and 16 tested orders for the expanded and reduced datasets, respectively. These significant differences predominantly involved faster rates in high-latitude limits (16 out of 17 and 10 out of 12 for the expanded and reduced datasets, respectively). At the family level, significant rate differences were detected in 36 and 17 families out of the 41 and 27 tested for the expanded and reduced datasets, respectively (Table S3). Again, significant differences predominantly involved faster rates in high-latitude limits (33 versus 3 and 13 versus 4 for the expanded and reduced datasets, respectively). Therefore, although not universal, a faster rate of evolution of high-latitude range limits is widespread among marine fish lineages. Finally, contrary to the expectation based on Rapoport’s rule, in general there was a negative relationship between latitude and latitudinal range (Figure 3), which was significant in 11 out of 15 orders (Table 2) and 19 out of 23 families for the reduced dataset (Table S4). There was no case of the positive relationship between latitude and latitudinal range predicted by Rapoport’s rule for any of the tested orders and families.

Figure 3.
Figure 3.

Latitudinal variation in the northern limit (A), median (B), and southern limit (C) of marine fishes, as well as the latitudinal distribution of their corresponding latitudinal range sizes.

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Table 1.

Relative fit of models in which high- and low-latitude range limits of marine fish orders evolve at the same or different rates: likl: log likelihood of multiple-rate model; lik2: likelihood of single-rate model; σ2 high and σ2 low indicate estimated rates of evolution for high- and low-latitude range limits, respectively; N: number of analyzed species. Values for the expanded dataset indicate medians across 100 alternative topologies. Bold-face rates are significantly different.

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Table 2.

Phylogenetic generalized least squared analyses of the relationship between absolute latitude and latitudinal range of different fish orders.

It is important to note that, given that the Atlantic and Indo-Pacific ocean basins were influenced by different histories and environmental gradients, we repeated our analyses separately for evolutionary rate tests, and considered whether species were present in either (or both) ocean basins as a covariate in PGLS analyses. Rate tests provided qualitatively similar results (Table S5 for orders, Table S6 for families). Likewise, the PGLS for different families (Table S7) and orders (Table S8) did not show a significant effect of ocean basin on the relationship between latitude and latitudinal range except for the order Perciformes and the family Scorpaenidae. However, when the corresponding data were visualized (Figure S2), it becomes clear that the significant effect of ocean basin on Perciformes is mostly due to species with very large range sizes that occur in both basins whose range size is not related to latitude (Figure S2). Although there was also a significant effect of ocean basin on the scorpaenid range data, it was mostly reflected in different slopes of relationships that were still negative, thus corroborating that none of the studied fish taxa showed evidence for a positive relationship between range size and latitude that is expected based on Rapoport’s rule.

DISCUSSION

In this study we provide the most comprehensive assessment of the evolution of latitudinal ranges of marine fishes to date. In particular, we uncover several general principles governing geographical range evolution in reef-associated fishes, namely (1) there was stronger phylogenetic signal in latitudinal midpoint than in latitudinal limits; (2) high-latitude range limits evolve substantially faster than low-latitude range limits; and (3) latitudinal range sizes tend to become larger in species whose medians are closer to the equator.

The detection of phylogenetic signal in traits related to geographical ranges might provide insight into important mechanisms driving their evolution. For instance, if closely related species show range overlap, they could experience similar conditions that would lead to expansions and contractions in their geographical ranges in parallel when faced with climate change, as seems to be the case in birds (Mouillot & Gaston, 2009). However, our results indicate that not all properties of reef fish latitudinal ranges share similar levels of phylogenetic signal. Rather, range medians tended to show higher phylogenetic signal than either latitudinal range or limits. These differences suggest that the evolution of latitudinal ranges takes place at a relatively constant rate, whereas range size and limits might experience stronger heterotachy, thus obscuring patterns of phylogenetic autocorrelation. These results are particularly intriguing when compared to the estimates of evolutionary rates (Table 1, Table S3). The combination of relatively lower phylogenetic signal in high-latitude range limits and their higher evolutionary rates is not obvious, given that higher rates do not necessarily entail lower phylogenetic signal (Revell et al., 2008). Rather, these results provide a scenario in which tropical reef fish gradually change the median position and site of their latitudinal ranges, whereas range limits (particularly those at higher latitudes) show a faster and more heterogeneous rate of evolution. One potential mechanism to explain this pattern is the observation that higher latitudes have experienced more variation in temperatures through time (Siqueira et al., 2016; Gaboriau et al., 2019). More detailed studies, particularly using more precise geographical distribution data, as well as more detailed phylogenetic comparative methods of range evolution, might provide important insight into the extent to which this scenario is representative of reef fish range evolution in general.

We confirmed previous studies suggesting an inverse Rapoport rule for marine fishes (Rohde et al., 1993; Macpherson & Duarte, 1994). It is important to note that Macpherson (2003) and Fortes & Absalão (2010) actually found patterns consistent with Rapoport’s rule in smaller and larger datasets than ours, respectively, of marine fishes. However, they used the method proposed by Stevens (1989), which compares the mean latitudinal range of all species within each 5° latitudinal band within the latitudinal gradient. As indicated by Rohde et al. (1993), in this method the same species are counted multiple times as they are distributed across different latitudinal bands, leading to statistical issues of nonindependence (see also Rohde & Heap, 1996; Ribas & Schoereder, 2006). Interestingly, an inverse Rapoport’s rule was also found for marine prosobranch gastropods living on the shelves of the western Atlantic and eastern Pacific Oceans (Roy et al., 1998) and for marine bivalves in the western and eastern Pacific and western Atlantic coasts (Tomašových et al., 2015). The reverse Rapoport’s rule appears to be common among marine organisms because of the nonlinearity of the latitudinal gradient of temperature in the sea, with much weaker spatial variation in annual minimum, mean and maximum daily temperature at low than at mid latitudes. These effects may be a general factor shaping latitudinal gradients in range size, because at the global scale, as shallow thermal gradients within the tropics and steep thermal gradients at higher latitudes also characterize some terrestrial environments (Tomašových et al., 2015).

To what extent do latitudinal ranges in marine and terrestrial organisms evolve according to the same rules? Other than the fact that latitudinal ranges of marine organisms are commonly considered much larger than those of terrestrial organisms (Gaston, 2003), there have been few attempts to assess the extent to which geographical range evolution might differ between these two environments. We argue that, despite the obvious differences between marine and terrestrial life, their geographical ranges actually share several important characteristics, namely (1) approximately lognormal distributions with a left skew (Gaston, 2003; Macpherson, 2003; Mora & Robertson, 2005; Figure 1); (2) phylogenetic signal in geographical range properties (Cardillo, 2015; Pie & Meyer, 2017; Figure 2, Figure S1, Tables S1, S2); (3) asymmetry in evolutionary rates between high- and low-latitude limits (Pie & Meyer, 2017; Table 1, Table S3). Although these characteristics seem to represent general principles regarding geographical range evolution that transcend differences between land and ocean habitats, there are several taxa that seem to depart from this expectation. Therefore, one of the main contributions of our study is that we can now actually recognize those taxa as exceptional, and we can now seek to understand why they are not constrained by the same mechanisms as other taxa.

There are some important caveats with respect to our analyses. For instance, we have not explicitly considered differences among species with respect to depth, which might be an important confounding factor for marine fish (e.g. Macpherson & Duarte, 1994). However, in the case of reef fishes, depth does not seem to play an important role in explaining interspecific variation in range size (Luiz et al., 2012, 2013). It is also important to note that our estimates of rates of evolution depend fundamentally on (1) the accuracy of the phylogenetic relationships between the studied species and (2) the extent to which distribution ranges evolve according to a Brownian motion model. Formally assessing phylogenetic accuracy is a challenging task, particularly for large-scale phylogenies with thousands of species, in which the level of topological error might vary across lineages based on the level of phylogenetic and taxonomic sampling. Such inaccuracies have been shown to affect downstream analyses (e.g. Title & Rabosky, 2019). We concede that some level of error is present in the phylogenetic relationships used in the present study, particularly when using phylogenetic imputation (Chang et al., 2020). However, we believe that such inaccuracies are unlikely to alter our conclusions for three main reasons. First, any error in the analyzed phylogenies would lead to undirected random noise as opposed to differentially overestimating high-latitude limits in relation to low-latitude limits, which would in fact cause the estimated rate differences to be conservative. Second, the consistency in the results across fish taxa of widely different ecologies and biogeographical distributions (and with terrestrial organisms as well) would be unlikely due to chance alone. Finally, the sensitivity analyses carried out in our study, varying the phylogenies in both the expanded and reduced datasets, indicates that our conclusions are largely unaffected by the topological variation in the underlying trees. With respect to the adequacy of Brownian motion (BM) as a model of range evolution, we can most certainly say that it is not. For instance, BM assumes that species are identical in their trait values at the time of speciation, which would be unrealistic for all but some specific cases of sympatric speciation. Also, BM is unbounded, whereas ranges are bounded both by continents and by the poles. However, our goal was not to provide a realistic model of range size but rather a first approximation to estimate rates of range size evolution. At the present, there are adaptations of BM-like processes to model specifically the evolution of geographical ranges. We hope that our results, particularly the asymmetry in the evolutionary rates between low- and high-latitude limits, would become an important component of such models in the future.

Supplementary material

Figure S1.
Figure S1.

Phylogenetic signal, according to Pagel’s λ (Pagel 1999), of properties of geographical ranges of tropical reef fish families. Details on estimates, corresponding likelihoods and p-values are indicated in Table S2.

Figure S2.
Figure S2.

Relationship between latitudinal range size (ln-transformed) and latitudinal position for the clades for which Ocean basin had a significant effect, based on PGLS analyses. We only tested taxa that had at least 10 tips in each of the groups.

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Table S1.

Tests of phylogenetic signal of latitudinal range size, lower latitude, median and higher latitude limits for different reef fish families.

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Table S2.

Tests of phylogenetic signal of latitudinal range size, lower latitude, median and higher latitude limits for different reef fish orders.

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Table S3.

Relative fit of models in which high- and low-latitude range limits of marine fish families evolve at the same or different rates: likl: log likelihood of multiple-rate model; lik2: likelihood of single-rate model; σ2 high and σ2 low indicate estimated rates of evolution for high- and low-latitude range limits, respectively; N: number of analyzed species. Values for the expanded dataset indicate medians across 100 alternative topologies. Bold-face rates are significantly different.

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Table S4.

Phylogenetic generalized least squares analyses of the relationship between absolute latitude of the range median and latitudinal range of different fish orders

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Table S5.

Relative fit of models in which high- and low-latitude range limits of marine fish orders evolve at the same or different rates, analyzing separately each ocean basin: likl: log likelihood of multiple-rate model; lik2: likelihood of single-rate model; σ2 high and σ2 low indicate estimated rates of evolution for high- and low-latitude range limits, respectively; N: number of analyzed species. Values for the expanded dataset indicate medians across 100 alternative topologies. Bold-face rates are significantly different.

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Table S6.

Relative fit of models in which high- and low-latitude range limits of marine fish families evolve at the same or different rates, analyzing separately each ocean basin: lik1: log likelihood of multiple-rate model; lik2: likelihood of single-rate model; σ2 high and σ2 low indicate estimated rates of evolution for high- and low-latitude range limits, respectively; N: number of analyzed species. Values for the expanded dataset indicate medians across 100 alternative topologies. Bold-face rates are significantly different.

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Table S7.

Phylogenetic generalized least squares analyses of the relationship between absolute latitude of the range median and latitudinal range of different fish orders using ocean basin as a covariate.

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Table S8.

Phylogenetic generalized least squares analyses of the relationship between absolute latitude of the range median and latitudinal range of different fish families using ocean basin as a covariate.

ACKNOWLEDGMENTS

This paper is developed in the context of National Institutes for Science and Technology (INCT) in Ecology, Evolution and Biodiversity Conservation, supported by MCTIC/CNPq (proc. 465610/2014-5) and FAPEG (proc. 201810267000023). MRP was partially funded by a grant from CNPq/MCT (301636/2016-8).

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Posted November 04, 2020.
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The evolution of latitudinal range limits in tropical reef fishes: heritability, limits, and inverse Rapoport’s rule
Marcio R. Pie, Raquel Divieso, Fernanda S. Caron, Alexandre C. Siqueira, Diego R. Barneche, Osmar J. Luiz
bioRxiv 2020.11.02.365700; doi: https://doi.org/10.1101/2020.11.02.365700
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