Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes

© 2018 Hing et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Social organization is a key factor influencing a species’ foraging and reproduction, which may ultimately affect their survival and ability to recover from catastrophic disturbance. Severe weather events such as cyclones can have devastating impacts to the physical structure of coral reefs and on the abundance and distribution of its faunal communities. Despite the importance of social organization to a species’ survival, relatively little is known about how major disturbances such as tropical cyclones may affect social structures or how different social strategies affect a species’ ability to cope with disturbance. We sampled group sizes and coral sizes of group-forming and pair-forming species of the Gobiid genus Gobiodon at Lizard Island, Great Barrier Reef, Australia, before and after two successive category 4 tropical cyclones. Group sizes of group-forming species decreased after each cyclone, but showed signs of recovery four months after the first cyclone. A similar increase in group sizes was not evident in group-forming species after the second cyclone. There was no change in mean pair-forming group size after either cyclone. Coral sizes inhabited by both group- and pair-forming species decreased throughout the study, meaning that group-forming species were forced to occupy smaller corals on average than before cyclone activity. This may reduce their capacity to maintain larger group sizes through multiple processes. We discuss these patterns in light of two non-exclusive hypotheses regarding the drivers of sociality in Gobiodon, suggesting that benefits of philopatry with regards to habitat quality may underpin the formation of social groups in this genus

Book Review on The Philosophical Challenge from China (Edited by Brian Bruya)

In this paper, I review the book The Philosophical Challenge from China, edited by Brian Bruya. I critically discuss each of the 13 contributions

Molecular phylogeny, temporal patterns of lineage diversification and phylogeography of the surgeonfish genus Naso (Acanthuridae)

A species-level phylogeny was constructed for all described (19) Naso species (Family: Acanthuridae) using three markers in combination, one nuclear (ETS2) and two mitochondrial (16S rRNA and cytochrome b). A number of taxa representing species from all acanthurid genera were included to generate a genus-level (total of 38 species) phylogeny of the order Acanthuroidei (surgeonfishes). Maximum likelihood, maximum parsimony and Bayesian inference analyses produced similar tree topologies, which confirmed the previously proposed genus-level relationships and resolved for the first time inter-specific relationships of all species of the monophyletic genus Naso. Species of the genus Naso segregated into four major sub-clades, with members of the subgenus Axinurus appearing basal. This molecular phylogeny was then used to examine hypotheses about the evolutionary relationships among species of Naso. This study demonstrates that distinct foraging modes and specialised body shapes arose independently at different times in the evolutionary history of the genus. Members of the subgenus Axinurus, characterised by a scombriform morphology, caudal fin structure and pelagic foraging mode, were consistently placed basal to the remaining Naso species, suggesting that pelagic foraging is plesiomorphic and benthic foraging derived in this genus. The genus-level phylogeny (nuclear marker, ETS2) was used to obtain a range of age estimates for the most recent common ancestor of the genus Naso. These age estimates (range of 52MY to 43.3MY) were then used to estimate divergence times (by nonparametric rate smoothing method) of the nodes, giving rise to extant Naso species using the combined sequence data (from all loci). The reconstruction of the pattern of divergence of extant species indicates two sequences of events. The basal species characterised by pelagic foraging modes arose during the Eocene and Oligocene. Most of the remaining Naso species, including those characterised by benthic foraging, arose over a period of 20MY during the Miocene. Diversification during this period was associated with major plate tectonic and glaciation events, resulting in changes in sea level, ocean temperature and productivity regimes. To examine further speciation events and the underlying processes, several comparative phylogeographic studies were undertaken. For this purpose, a Naso-specific fast evolving mitochondrial marker was designed from the control region (d-loop). Firstly, a widely distributed species N. vlamingii, was selected to examine genetic connectivity and diversity throughout its distribution in the Indo-Pacific Ocean. Although very weak (overall Fst 0.005) genetic differentiation was obtained for this species over its sampled range, suggesting gene flow, there was some evidence of isolation by distance at the largest spatial scale (between Seychelles and the Philippines). This however, may be due to lack of samples from the Indian Ocean. There was no subdivision into distinct geographic regions, hence no evidence of cryptic speciation across the range sampled in this study, despite the presence of the central Indian Ocean barrier in its distribution range. Diversity indices (haplotype, h and nucleotide, p) were extremely high (h = 1.0 and p = 15.1%), indicating that this species has had a long, but unstable evolutionary history, which has repeatedly allowed populations to diverge in isolation and to make secondary contact subsequently. A haplotype tree identified deep divergences for this species, suggesting that isolated populations diverged at times of low sea level. The lack of geographic partitioning in this species suggests that secondary contact was made between previously isolated and divergent populations at times of elevated sea level. The high dispersive capacity of the species is what allows secondary contact to occur between temporarily isolated populations. Additionally, two sister species pairs were selected for comparative phylogeographic studies. One pair (N. lituratus– N. elegans) spanned the same distribution range as N. vlamingii, but the species pair was partitioned by ocean basins across this range (Indian- /Pacific Ocean). The second pair (N. tuberosus – N. tonganus) has an even more restricted distribution range (west Indian-/west Pacific Ocean) and was also partitioned by ocean basins. The two sister species diverged allopatrically, and species of both sister pairs (N. lituratus– N. elegans and N. tuberosus – N. tonganus) segregated into distinct clades. There was no distinct geographic subdivision throughout the sampling range for any of these species. Instead, low levels of genetic differentiation were recorded among populations of each species (overall Fst values ranged from 0.005 to - 0.001) suggesting high levels of gene flow. Despite the presence of gene flow among populations there was some indication of reduced gene flow across the Indian Ocean (between Amirante of Seychelles and Cocos Keeling Island) for N. elegans. There was no indication of gene flow between species in either of the sister pairs (N. lituratus – N. elegans Fst =0.75 and N. tuberosus – N. tonganus Fst =0.71), despite the fact that each pair was considered a single species as recently as 2001 and 2002 respectively. This indicates reproductive isolation, despite the potential for extensive dispersal in these species. The diversity indices were high for all of the species (h = 0.90 – 1.00, p = 9.0 – 11.6%; h = 1.00, p = 4.2 – 6.4% respectively), indicating deep divergences between haplotypes, as was the case for N. vlamingii. Several factors probably contribute to the population genetic structure of all five species: certain life history traits such as an extensive pelagic larval duration (up to 3 months) in combination with the ability of larvae to swim actively for extended periods, their long evolutionary history, the longevity (reach 30 – 40 years) and relatively short time to reach reproductive maturity coupled with overlapping generations (offspring) reproducing. The dispersive capacities of N. vlamingii are clearly the greatest of the five species studied, and may be attributed to the semi-pelagic adult lifestyle combined with the pelagic larval duration and a generalist dietary habit of this species. This study has demonstrated that by applying a hierarchical approach (phylogenetic, temporal, and phylogeographic) in combination with biological, ecological and historical perspectives, it has been possible to elucidate the processes important in the diversification of the genus Naso

Molecular phylogeny, temporal patterns of lineage\ud diversification and phylogeography of the surgeonfish genus\ud Naso (Acanthuridae)

A species-level phylogeny was constructed for all described (19) Naso species (Family:\ud Acanthuridae) using three markers in combination, one nuclear (ETS2) and two\ud mitochondrial (16S rRNA and cytochrome b). A number of taxa representing species\ud from all acanthurid genera were included to generate a genus-level (total of 38 species)\ud phylogeny of the order Acanthuroidei (surgeonfishes). Maximum likelihood, maximum\ud parsimony and Bayesian inference analyses produced similar tree topologies, which\ud confirmed the previously proposed genus-level relationships and resolved for the first\ud time inter-specific relationships of all species of the monophyletic genus Naso. Species\ud of the genus Naso segregated into four major sub-clades, with members of the subgenus\ud Axinurus appearing basal. This molecular phylogeny was then used to examine\ud hypotheses about the evolutionary relationships among species of Naso. This study\ud demonstrates that distinct foraging modes and specialised body shapes arose\ud independently at different times in the evolutionary history of the genus. Members of\ud the subgenus Axinurus, characterised by a scombriform morphology, caudal fin\ud structure and pelagic foraging mode, were consistently placed basal to the remaining\ud Naso species, suggesting that pelagic foraging is plesiomorphic and benthic foraging\ud derived in this genus.\ud The genus-level phylogeny (nuclear marker, ETS2) was used to obtain a range of age\ud estimates for the most recent common ancestor of the genus Naso. These age estimates\ud (range of 52MY to 43.3MY) were then used to estimate divergence times (by\ud nonparametric rate smoothing method) of the nodes, giving rise to extant Naso species\ud using the combined sequence data (from all loci). The reconstruction of the pattern of\ud divergence of extant species indicates two sequences of events. The basal species\ud characterised by pelagic foraging modes arose during the Eocene and Oligocene. Most\ud of the remaining Naso species, including those characterised by benthic foraging, arose\ud over a period of 20MY during the Miocene. Diversification during this period was\ud associated with major plate tectonic and glaciation events, resulting in changes in sea\ud level, ocean temperature and productivity regimes.\ud To examine further speciation events and the underlying processes, several comparative\ud phylogeographic studies were undertaken. For this purpose, a Naso-specific fast evolving mitochondrial marker was designed from the control region (d-loop). Firstly, a\ud widely distributed species N. vlamingii, was selected to examine genetic connectivity\ud and diversity throughout its distribution in the Indo-Pacific Ocean. Although very weak\ud (overall Fst 0.005) genetic differentiation was obtained for this species over its sampled\ud range, suggesting gene flow, there was some evidence of isolation by distance at the\ud largest spatial scale (between Seychelles and the Philippines). This however, may be\ud due to lack of samples from the Indian Ocean. There was no subdivision into distinct\ud geographic regions, hence no evidence of cryptic speciation across the range sampled in\ud this study, despite the presence of the central Indian Ocean barrier in its distribution\ud range. Diversity indices (haplotype, h and nucleotide, p) were extremely high (h = 1.0\ud and p = 15.1%), indicating that this species has had a long, but unstable evolutionary\ud history, which has repeatedly allowed populations to diverge in isolation and to make\ud secondary contact subsequently. A haplotype tree identified deep divergences for this\ud species, suggesting that isolated populations diverged at times of low sea level. The lack\ud of geographic partitioning in this species suggests that secondary contact was made\ud between previously isolated and divergent populations at times of elevated sea level.\ud The high dispersive capacity of the species is what allows secondary contact to occur\ud between temporarily isolated populations.\ud Additionally, two sister species pairs were selected for comparative phylogeographic\ud studies. One pair (N. lituratus– N. elegans) spanned the same distribution range as N.\ud vlamingii, but the species pair was partitioned by ocean basins across this range (Indian-\ud /Pacific Ocean). The second pair (N. tuberosus – N. tonganus) has an even more\ud restricted distribution range (west Indian-/west Pacific Ocean) and was also partitioned\ud by ocean basins. The two sister species diverged allopatrically, and species of both\ud sister pairs (N. lituratus– N. elegans and N. tuberosus – N. tonganus) segregated into\ud distinct clades. There was no distinct geographic subdivision throughout the sampling\ud range for any of these species. Instead, low levels of genetic differentiation were\ud recorded among populations of each species (overall Fst values ranged from 0.005 to -\ud 0.001) suggesting high levels of gene flow. Despite the presence of gene flow among\ud populations there was some indication of reduced gene flow across the Indian Ocean\ud (between Amirante of Seychelles and Cocos Keeling Island) for N. elegans. There was no indication of gene flow between species in either of the sister pairs (N.\ud lituratus – N. elegans Fst =0.75 and N. tuberosus – N. tonganus Fst =0.71), despite the\ud fact that each pair was considered a single species as recently as 2001 and 2002\ud respectively. This indicates reproductive isolation, despite the potential for extensive\ud dispersal in these species. The diversity indices were high for all of the species (h = 0.90\ud – 1.00, p = 9.0 – 11.6%; h = 1.00, p = 4.2 – 6.4% respectively), indicating deep\ud divergences between haplotypes, as was the case for N. vlamingii. Several factors\ud probably contribute to the population genetic structure of all five species: certain life\ud history traits such as an extensive pelagic larval duration (up to 3 months) in\ud combination with the ability of larvae to swim actively for extended periods, their long\ud evolutionary history, the longevity (reach 30 – 40 years) and relatively short time to\ud reach reproductive maturity coupled with overlapping generations (offspring)\ud reproducing. The dispersive capacities of N. vlamingii are clearly the greatest of the five\ud species studied, and may be attributed to the semi-pelagic adult lifestyle combined with\ud the pelagic larval duration and a generalist dietary habit of this species.\ud This study has demonstrated that by applying a hierarchical approach (phylogenetic,\ud temporal, and phylogeographic) in combination with biological, ecological and\ud historical perspectives, it has been possible to elucidate the processes important in the\ud diversification of the genus Naso

Acquiring reef fish DNA sequences from formalin-fixed museum specimens

In recent years molecular techniques have invaded the marine realm. These techniques are mainly used to determine phylogenetic relationships between species, and for population genetic and phylogeographic studies. The use of museum specimens is advantageous, especially for phylogenetic studies. It enables sampling of species that are extinct or endangered, and those that are difficult to obtain fresh from the wild. Such specimens may be quite old (from collections at the beginning of the 20th century) and are generally fixed in formalin (10%) prior to being preserved in alcohol. The general consensus is that formalin-fixed tissue cannot be used for DNA studies, as yields are very low and DNA is substantially degraded (Dillon et al., 1996; Wirgin et al., 1997). However, a few studies described and compared DNA extractions from different preservation techniques, including formalin-fixed specimens of tapeworms (Li et al., 2000), trout (Shiozawa et al., 1992), Atlantic coast bass (Wirgin et al., 1997), molluscs (Chase et al., 1998), a range of other taxa (amphibian, reptile, fish, invertebrate; Shedlock et al., 1997), and insects (Dillon et al., 1996). All of these studies, with the exception of the last one, successfully extracted mitochondrial DNA from formalin-fixed samples. The protocol we developed to extract DNA from mitochondrial and nuclear DNA from museum collections of reef fish, focused on the genera Naso (Family: Acanthuridae), Scams and Chlorurus (Family: Scaridae). Here we present this method for DNA extractions from formalin-fixed reef fish specimens, subsequent PCR (polymerase chain reaction) amplification, and sequencing of such samples. The technique described here differs from the above studies in its detailed methodology, including extraction time and chemicals used. Furthermore, it compares the differences for PCR optimization and amplification between ethanol-preserved (fresh) and formalin-fixed tissues. This study is the first to document successful sequencing of a nuclear marker from formalin-fixed samples

Patterns of lineage diversification in the Genus Naso (Acanthuridae)

The evolutionary history of the reef fish genus Naso (F. Acanthuridae) was examined using a complete species-level molecular phylogeny of all recognized (19) species based on three loci (one nuclear ETS2 and two mitochondrial 16S, cyt b). This study demonstrates that distinct foraging modes and specialized body shapes arose independently at different times in the evolutionary history of the genus. Members of the subgenus Axinurus, characterized by a scombriform morphology, caudal fin structure and pelagic foraging mode, were consistently placed basal to the remaining Naso species, suggesting that pelagic foraging is plesiomorphic and benthic foraging derived in this genus. We used a genus-level phylogeny (nuclear marker, ETS2), which included several taxa from all other acanthurid genera, to obtain a range of age estimates for the most recent common ancestor of the genus Naso. These age estimates (range of 52–43.3 MY) were then used to estimate divergence times (by nonparametric rate smoothing method) of the node giving rise to extant Naso species using the combined sequence data (from all loci). The reconstruction of the pattern of divergence of extant species indicates two sequences of events. The basal species characterized by pelagic foraging modes arose during the Eocene and Oligocene. Most of the remaining Naso species, including those characterized by benthic foraging, arose over a period of 20 MY during the Miocene. Diversification during this period was associated with major plate tectonic and glaciation events, resulting in changes in sea level, ocean temperature and productivity regimes. Regardless of the foraging mode exhibited, all species of Naso have a caudal propulsive unit similar to that observed in pelagic scombriform fishes, a legacy of the basal position of the subgenus Axinurus in the phylogeny of the genus

Delayed recovery and host specialization may spell disaster for coral-fish mutualism

Mutualisms are prevalent in many ecosystems, yet little is known about how symbioses are affected by ecological pressures. Here, we show delayed recovery for 13 coral-dwelling goby fishes (genus Gobiodon) compared with their host Acropora corals following four consecutive cyclones and heatwaves. While corals became twice as abundant in 3 years postdisturbances, gobies were only half as abundant relative to predisturbances and half of the goby species disappeared. Although gobies primarily occupied one coral species in greater abundance predisturbances, surviving goby species shifted hosts to newly abundant coral species when their previously occupied hosts became rare postdisturbances. As host specialization is key for goby fitness, shifting hosts may have negative fitness consequences for gobies and corals alike and affect their survival in response to environmental changes. Our study is an early sign that mutualistic partners may not recover similarly from multiple disturbances, and that goby host plasticity, while potentially detrimental, may be the only possibility for early recovery

Repeated cyclone events reveal potential causes of sociality in coral-dwelling Gobiodon fishes.

Social organization is a key factor influencing a species' foraging and reproduction, which may ultimately affect their survival and ability to recover from catastrophic disturbance. Severe weather events such as cyclones can have devastating impacts to the physical structure of coral reefs and on the abundance and distribution of its faunal communities. Despite the importance of social organization to a species' survival, relatively little is known about how major disturbances such as tropical cyclones may affect social structures or how different social strategies affect a species' ability to cope with disturbance. We sampled group sizes and coral sizes of group-forming and pair-forming species of the Gobiid genus Gobiodon at Lizard Island, Great Barrier Reef, Australia, before and after two successive category 4 tropical cyclones. Group sizes of group-forming species decreased after each cyclone, but showed signs of recovery four months after the first cyclone. A similar increase in group sizes was not evident in group-forming species after the second cyclone. There was no change in mean pair-forming group size after either cyclone. Coral sizes inhabited by both group- and pair-forming species decreased throughout the study, meaning that group-forming species were forced to occupy smaller corals on average than before cyclone activity. This may reduce their capacity to maintain larger group sizes through multiple processes. We discuss these patterns in light of two non-exclusive hypotheses regarding the drivers of sociality in Gobiodon, suggesting that benefits of philopatry with regards to habitat quality may underpin the formation of social groups in this genus

Uneven declines between corals and cryptobenthic fish symbionts from multiple disturbances

With the onset and increasing frequency of multiple disturbances, the recovery potential of critical ecosystem-building species and their mutual symbionts is threatened. Similar effects to both hosts and their symbionts following disturbances have been assumed. However, we report unequal declines between hosts and symbionts throughout multiple climate-driven disturbances in reef-building Acropora corals and cryptobenthic coral-dwelling Gobiodon gobies. Communities were surveyed before and after consecutive cyclones (2014, 2015) and heatwaves (2016, 2017). After cyclones, coral diameter and goby group size (i.e., the number of gobies within each coral) decreased similarly by 28–30%. After heatwave-induced bleaching, coral diameter decreased substantially (47%) and gobies mostly inhabited corals singly. Despite several coral species persisting after bleaching, all goby species declined, leaving 78% of corals uninhabited. These findings suggest that gobies, which are important mutual symbionts for corals, are unable to cope with consecutive disturbances. This disproportionate decline could lead to ecosystem-level disruptions through loss of key symbiont services to corals