Recent dispersal and diversification within the clingfish genus Acyrtus (Actinopterygii: Gobiesocidae), with the description of a new western Atlantic species

Thais L. Quintão1, João Luiz Gasparini3, Jean-Christophe Joyeux2, Luiz A. Rocha4 and Hudson T. Pinheiro4,5

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Abstract​


EN

The genus Acyrtus (Gobiesocidae) is represented by four valid species distributed in the western Atlantic, and a recently described fifth species from the eastern Pacific. Here, we describe a new species endemic to Trindade Island, Brazil, and provide the first phylogenetic inference for the genus including all representatives. The new species can be distinguished from all its congeners by meristic and morphometric characters, as well as genetic differences. It presents low genetic diversity and, contrarily to other Trindade Island endemic fishes, shows no evidence of recent population growth. Our phylogeny reveals cryptic species and the paraphyletic nature of Acyrtus, which included Arcos nudus (western Atlantic) in a clade that separated from Arcos erythrops (tropical eastern Pacific) around 20 Mya. The three species found in the Brazilian Province, including one that remains undescribed, form a monophyletic clade which colonized the western South Atlantic around 2.6 Mya. Our study suggests that Arcos nudus should be placed in Acyrtus, and that the relationships among the closely-related Gobiesocidae genera Acyrtus (mostly from the Atlantic Ocean) and Arcos (from the Pacific Ocean) need further investigation.

Keywords: Brazilian Province, Endemism, Evolution, Phylogeny, Reef fish.

PT

O gênero Acyrtus (Gobiesocidae) é representado por quatro espécies válidas encontradas no Atlântico ocidental e uma recentemente descrita do Pacífico oriental. Aqui descrevemos uma nova espécie endêmica da Ilha da Trindade, Brasil, e apresentamos a primeira inferência filogenética para o gênero incluindo todos os representantes. A nova espécie pode ser distinguida de suas congêneres por caracteres merísticos e morfométricos, bem como por diferenças genéticas. A espécie apresenta baixa diversidade genética, entretanto, diferentemente de outras espécies endêmicas da Ilha da Trindade, não mostra evidência de expansão populacional recente. A filogenia obtida revelou a existência de espécies crípticas e a natureza parafilética de Acyrtus, o qual inclui Arcos nudus (do Atlântico ocidental), e que é separado de Arcos erythrops (do Pacifico tropical oriental) por cerca de 20 milhões de anos. As três espécies encontradas no Brasil, incluindo uma ainda não descrita, formam um clado monofilético que colonizou o Atlântico Sul ocidental há cerca de 2,6 milhões de anos. Nosso estudo sugere que Arcos nudus deva ser alocado no gênero Acyrtus, e que as relações entre os gêneros Acyrtus (em maioria do Oceano Atlântico) e Arcos (do Oceano Pacífico) precisam ser estudadas em mais detalhes.

Palavras-chave: Endemismo, Evolução, Filogenia, Peixes recifais, Província Brasileira.

Introduction​


The cryptobenthic fish family Gobiesocidae (sensu Brandl et al., 2018), commonly known as clingfishes, comprises 190 recognized species (Fricke et al., 2022) distributed in freshwater, brackish, and coastal areas of the world’s tropical and subtropical regions (Briggs, 1955; Conway et al., 2017). Although occupying different environments and microhabitats (Gonçalves et al., 2002; Henriques et al., 2002), including a wide bathymetric range (Sparks, Gruber, 2012; Fricke et al., 2017), many species are morphologically similar and there is recognized uncertainty in their classification (Conway et al., 2020).

In this context, the use of molecular approaches combined with traditional taxonomy has provided a better understanding of evolutionary relationships (e.g., Henriques et al., 2002; Fricke et al., 2017; Wagner et al., 2019) and identification of cryptic lineages (e.g., Henriques et al., 2002;Craig, Randall, 2008; Conway et al., 2014; Wagner et al., 2019; Torres-Hernández et al., 2020). Though recent molecular studies have provided important progress in the knowledge of this family (Conway et al., 2017, 2020; Fricke et al., 2017), the evolutionary history of most species and the full extent of Gobiesocidae diversity remain unknown. Phylogenetic work including the New World Gobiesocinae suggested a recent diversification, the presence of several cryptic species and paraphyletic genera (Conway et al., 2014, 2017, 2020; Tavera et al.,2021), all of which we will explore in this study within the genus Acyrtus Schultz, 1944.

Acyrtus is represented by five valid species, Acyrtus artius Briggs, 1955, Acyrtus lanthanum Conway, Baldwin & White, 2014, Acyrtus pauciradiatus Sampaio, Anchieta, Nunes & Mendes, 2004 and Acyrtus rubiginosus (Poey, 1868) are restricted to the western Atlantic, while Acyrtus arturo Tavera, Rojas-Vélez & Londoño-Cruz, 2021, was recently described from the eastern Pacific. These are small-bodied fishes (maximum size of less than 30 mm) with cryptobenthic habits, some presenting large secretory cells similar to those present in the venom glands of other teleost fishes (Conway et al., 2014). In the Atlantic, three species are found in the Caribbean and the fourth (A. pauciradiatus) is endemic to Fernando de Noronha Archipelago and Rocas Atoll, in Brazil. However, two other undescribed species have been found in restricted locations of the southwestern Atlantic, one on the Brazilian continental shelf and the other in the oceanic Trindade Island (Pinheiro et al., 2017).

Morphologically, Acyrtus is closely related to Rimicola Jordan & Evermann, 1896, a genus restricted to the eastern Pacific. However, a recent molecular phylogenetic study exploring Gobiesocidae has shown a close relationship between Acyrtus and Arcos Schultz, 1944 and, under low bootstrap values, has placed Arcos nudus (Linnaeus, 1758), from the western Atlantic, within the Acyrtus clade (Conway et al., 2014). This result agrees with the distribution of Arcos and Acyrtus genera since Arcos is mainly restricted to the eastern Pacific and Acyrtus to the western Atlantic. However, the recent description of A. arturo (Tavera et al., 2021) from Malpelo Island opens discussion about the evolutionary history of Acyrtus and Arcos. In addition, both genera share morphological characteristics that obscure their evolutionary proximity (e.g., Tavera et al., 2021). Species of both genera have previously been described as Gobiesox (Schultz, 1944; Conway et al., 2017), indicating that morphological similarities often lead to misidentifications (Conway et al., 2017). In this study, we provide the first phylogenetic inference for the genus Acyrtus containing all known species and including the undescribed species from Trindade Island as new, and an undescribed species from Brazilian coast. In addition, we analyzed the evolutionary history of the genus, and the phylogeographic and demographic history of the Brazilian species complex.

Material and methods


Morphological analysis. The eight type specimens were collected with hand nets during a field expedition to Trindade Island in June 2009. Specimens were fixed in formalin 10% for 24 h, and then transferred to alcohol 70%. Counts were performed with a stereo microscope (Leica S9i, Amplification 6.1–55x) and X-rays obtained with a radiography system Faxitron LX60. Morphological characters were measured to the nearest 0.01 mm using an ocular micrometer mounted on a dissecting scope. Measurements and counts followed the methods presented in Briggs (1955), with the addition of predorsal and preanal lengths, which are the shortest distances between the tip of the upper lip and the dorsal and anal-fin origin, respectively (see Conway et al., 2014). Vertebral counts are presented as precaudal + caudal. The anterior-most vertebra with a haemal spine was counted as the first caudal vertebra, the urostylar complex the last. Following Smith-Vaniz (1971), the principal caudal ray counts included only those rays that articulate with the hypural plate, and are provided as upper+lower counts. Procurrent caudal rays are also provided as upper+lower counts. Measurements are expressed as a percentage of either standard length (SL) or head length (HL). Type specimens were deposited in the fish collections of Universidade Federal do Espírito Santo, Vitória (CIUFES), California Academy of Sciences, San Francisco (CAS-ICH), Museu Nacional do Rio de Janeiro, Rio de Janeiro (MNRJ), Museu de Zoologia da Universidade de São Paulo, São Paulo (MZUSP), Instituto de Biodiversidade e Sustentabilidade – NUPEM, Universidade Federal do Rio de Janeiro, Macaé (NPM), and Museu de Zoologia da Universidade Estadual de Campinas “Prof. Dr. Adão José Cardoso” (ZUEC). In the Description section, counts, measurements, and proportions of the holotype are followed by the range for paratypes inside parentheses. Teeth type and counts were obtained from a dissected specimen.

Genetic data. Cytochrome Oxidase I (COI) sequences of Acyrtus (A. artius, A. arturo, A. lanthanum, A. rubiginosus, Acyrtus sp.n., and Acyrtus sp.), Arcos (A. erythrops (Jordan & Gilbert, 1882)and A. nudus) and Gobiesox Lacepède, 1800 (G. maeandricus (Girard, 1858), G. punctulatus (Poey, 1876), and G. rhessodon Smith, 1881) were obtained from previous studies (Conway et al., 2014; Conway et al., 2017; Pinheiro et al., 2017; Tavera et al., 2021) and applied to phylogenetic and phylogeographic analyses. The DNA sequences from the Brazilian species A. pauciradiatus were extracted and amplified following protocols detailed in Weigt et al. (2012) for COI gene. Species of the families Gobiesocidae, Pseudochromidae, and Grammatidae were added as outgroups for the molecular-clock calibration. All sequences were aligned using ClustalW algorithm implemented in MEGA 7 (Kumar et al., 2016). Accession numbers of the sequences used are shown in Tab. S1.

Phylogenetic analysis and molecular clock calibration. Interspecific and intraspecific genetic divergences were calculated in MEGA 7 using Tamura-Nei model. Phylogenetic relationships among Acyrtus and Arcos were reconstructed by Bayesian Inference using Mr. Bayes 3.2.6 (Huelsenbeck, Ronquist, 1997). The analysis was performed for two parallel runs of 10 million generations, with four chains each and sampling trees every 1,000 generations. The burn-in value and the effective sample size (ESS) were assessed using Tracer 1.5 (Rambaut et al., 2018). All parameters exceed 200 in ESS values. The consensus tree was obtained from the maximum credibility clades with TreeAnnotator 1.7.5 (Drummond et al., 2012). The appropriate substitution model used was determined using PartitionFinder (Lanfear et al., 2017). We used SYM+I+G model for the first codon position, F81+I for the second position, and GTR+I+G for the third position. We used species of Gobiesox as outgroups based on Conway et al. (2017).

We estimated the divergence times among Acyrtus species using the Relaxed Clock Log Normal model and the Birth/Death prior implemented in BEAUTi & The BEAST 2.5.0 software (Bouckaert et al., 2014). Species of Gobiesocidae, Pseudochromidae, and Grammatidae family were incorporated in the alignment to implement a secondary calibration derived from the results of Near et al. (2013), which were also used by Conway et al. (2017) in the Gobiesocidae family phylogeny. We choose the nodes A (80.3 Ma), B (75.8 Ma), F (42.9 Ma), and G (23.1 Ma) from Conway et al. (2017) to represent the divergence of the last common ancestors between (A) Pseudochromidae + Grammatidae + Gobiesocidae, (B) Grammatidae + Gobiesocidae, (F) all Gobiesocidae species, and (G) Acyrtus + Arcos + Gobiesox. We constrained all node calibrations based on the topology obtained by Conway et al. (2017), which represents the most complete phylogeny obtained for the subfamily Gobiesocinae. The analysis was run in the Cipres Portal (http://www.phylo.org/) using 100 million generations and sampling every 3,000 generations. The effective sample size (ESS) and appropriate burn-in values were visualized in Tracer 1.5 (Rambaut et al., 2018). All parameters exceed 200 in ESS values. We used TreeAnnotator 1.4.3 (Drummond et al., 2012) to obtain the maximum clade credibility tree that was edited in FigTree (Rambaut, 2014) and Inkscape (Free Software Foundation, Boston, USA).

Phylogeographic analysis and demography. We calculated the genetic differentiation between Brazilian species (A. pauciradiatus, Acyrtus sp.n., and Acyrtus sp.) using the FST index (Wright, 1965) implemented in Arlequin 3.5.2.2 (Excoffier, Lischer, 2010). The COI haplotype network was constructed with the median-joining algorithm using PopArt (Bandelt et al., 1999). We performed demographic analysis only for Acyrtus sp.n. Haplotype and nucleotide diversity were estimated in DnaSP6 (Rozas et al., 2017) and neutrality tests were implemented in Arlequin 3.5.2.2. We used Tajima’s D and Fu’s F values to estimate possible events of population expansion. Finally, historical population dynamics were also evaluated using Bayesian Coalescent Skyline method implemented in Beast. We fixed the clock rate using the values obtained by the molecular clock analysis previously cited. The run comprised 10 million generations and samplings every 1,000 generations. We used Tracer 1.5 to check the parameters and to obtain the coalescent analysis output.

Results​


Acyrtus simon Gasparini & Pinheiro, new species

urn:lsid:zoobank.org:act:242B5ECF-E791-41DD-92E3-0BC8BA496910

(Fig. 1; Tab. 1)

Arcos sp. —Gasparini, Floeter, 2001:1646 [Trindade Island]. —Pereira-Filho et al., 2011:204 [Trindade Island]. —Simon et al., 2013:2123 [Trindade Island].

Acyrtus sp. —Macieira et al., 2015:390 [Trindade Island]. —Pinheiro et al., 2015:5 [Trindade Island]. —Pinheiro et al., 2017:83 [Trindade Island]. —Pinheiro et al., 2018:86 (Supplementary material) [Trindade Island]. —Guabiroba et al., 2020:701 [Martin Vaz Archipelago].

Acyrtus sp. nov. —Gasparini, 2017:78 [Trindade Island].

Holotype. CIUFES 2915, 26.41 mm SL, Brazil, Trindade Island, Calheta, 28 Jun 2009, H. T. Pinheiro & J. L. Gasparini (Fig. 1).

Paratypes. CAS-ICH 247280, 1, 22.21 mm SL; CIUFES 2914, 1, 26.00 mm SL; CIUFES 4448, 1 (dissected specimen), 32.23 mm SL; MNRJ 52794, 1, 24.71 mm SL; MZUSP 125855, 2, 21.81–25.44 mm SL; NPM 6839, 1, 25.79 mm SL; ZUEC 17336, 1, 30.60 mm SL, same data as for the holotype.

FIGURE 1 | Acyrtus simon, holotype CIUFES 2915, 26.41 mm SL. A. Specimen alive, photo taken by J. L. Gasparini in June 2009; BD. Specimen preserved, photo taken by R. M. Macieira on 31 October 2020. E. X-ray taken by M. M. Mincarone on 11 May 2022.

Diagnosis. Acyrtus simon differs from A. artius by having a deeper head depth (19–21% vs. 14–18% SL), a larger pelvic disc (36–39% vs. 29–36% SL), larger eye diameter (32–40% vs. 24–31% HL), and number of pectoral-fin rays (21–23 vs. 24–27) (Tabs. 1–2). Acyrtus simon can be distinguished from A. lanthanum by a deeper head depth (19–21% vs. 15–18% SL), larger eye diameter (32–40% vs. 24–31% HL), and number of pectoral-fin rays (21–23 vs. 24–25) (Tabs. 1–2). The new species differs from A. rubiginosus by a deeper head depth (19–21% vs. 13–16% SL), a larger pelvic disc (36–39% vs. 27–31% SL), wider pelvic disc (30–36% vs. 22–30% SL), larger eye diameter (32–40% vs. 23–28% HL), and number of pectoral-fin rays (21–23 vs. 24–27) (Tabs. 1–2). It differs from A. pauciradiatus by a larger pelvic disc (36–39% vs. 27–34% SL), shallower caudal peduncle (8–10% vs. 10–11% SL), longer caudal peduncle (10–17% vs. 5–8% SL), shorter anus–disc distance (6–12% vs. 12–13% SL), longer anus–anal fin distance (11–15% vs. 6–9% SL), longer snout length (20–33% vs. 9–15% HL), and narrower interorbital space (18–29% vs. 40–45% HL) (Tabs. 1–2). Acyrtus simon also differs from Acyrtus arturo by having shorter anus–disk distance (6–12 vs. 13–18% SL), longer anus–anal fin distance (11–15 vs. 4–9% SL), and longer snout length (20–33 vs. 10–15% HL) (Tabs. 1–2). It also differs from Arcos nudus [= Acyrtus nudus] by havinga different number of pectoral-fin rays (21–23 vs. 23–25) (Tab. 1).

TABLE 1 | Proportional measurements and counts of type specimens of Acyrtus simon. H = Holotype.

 

CIUFES 2915 (H)

CAS 247280

CIUFES 2914

MNRJ 52794

MZUSP 125855

MZUSP 125855

NUPEM 6839

ZUEC 17336

Total length (in mm)

32.19

26.94

30.91

30.26

32.94

26.50

31.68

36.38

Standard length (SL, in mm)

26.41

22.21

26.00

24.71

25.44

21.81

25.79

30.60

Measurements in % of SL

 

 

 

 

 

 

 

 

Head length

33.7

36.5

34.9

35.0

47.3

40.9

36.5

34.2

Head width

40.7

35.1

39.4

39.7

32.9

36.3

39.1

40.3

Head depth

20.1

18.8

20.5

20.5

19.2

19.2

21.1

19.9

Pelvic disc length

37.2

37.9

38.1

38.9

39.2

36.2

37.1

37.8

Pelvic disc width

34.6

30.3

34.6

35.6

33.6

34.3

32.8

35.6

Pre-dorsal distance

68.7

64.1

68.5

67.7

65.4

65.5

67.7

65.7

Pre-anal distance

71.2

71.2

74.6

72.1

70.2

71.9

71.8

71.6

dorsal length

17.3

20.7

14.3

16.5

20.9

16.4

18.4

15.7

Pectoral length

20.6

16.3

19.0

15.4

16.2

18.4

16.9

15.9

Caudal Peduncle length

12.9

09.5

15.0

14.6

16.9

11.0

12.0

10.8

Caudal peduncle depth

09.0

09.6

08.1

09.8

08.2

09.6

09.4

08.6

Anus-Disk distance

07.1

09.5

09.1

08.7

05.8

12.4

07.3

11.2

Anus-anal fin distance

11.4

11.5

12.9

13.4

12.1

12.7

14.5

11.5

Head length (HL, in mm)

8.91

8.12

9.09

8.65

12.05

8.94

9.43

10.47

Measurements in % of HL

 

 

 

 

 

 

 

 

Snout length

32.5

28.4

26.8

25.8

21.9

20.0

30.2

27.6

Eye diameter

40.1

38.0

36.5

35.7

32.9

32.2

39.6

39.9

Interorbital space

24.2

26.1

18.2

18.3

20.4

19.2

29.2

24.0

Counts

 

 

 

 

 

 

 

 

Dorsal-fin rays

8

9

9

8

8

9

9

8

Anal-fin rays

6

7

8

7

6

8

8

8

Principal caudal-fin rays

5+5

5+5

5+5

5+5

5+5

5+5

5+5

5+5

Procurrent caudal-fin rays

6+5

7+6

7+5

6+5

6+5

5+5

7+7

6+5

Pectoral-fin rays

21

22

23

22

21

23

25

23

Pelvic-fin rays

5

5

5

5

5

5

5

5

Vertebrae

12+17

11+18

12+17

12+17

12+17

12+17

12+17

13+16

 

Description. Meristic and proportional measurements of the holotype and seven paratypes given in Tab. 1. Dorsal-fin rays 8 (8–9). Anal-fin rays 6 (6–8). Principal caudal-fin rays 5+5. Procurrent caudal-fin rays 6 (5–7) + 5 (5–7). Pectoral-fin rays 21 (21–23; one with 25). Pelvic-fin rays I,4 (I, 4). Vertebrae 12 (11–13) + 17 (16–18). Body moderately depressed anteriorly, depth 4.9 (4.7–5.3) in SL. Head depressed, head width 2.4 (2.4–3.0) and head length 2.9 (2.1–2.9) in SL. Snout steep with a rounded outline, 3.1 (3.3–4.9) in head length. Posterior nostril surrounded by low fleshy rim and situated in front of anterior edge of eye; anterior nostril tubular, with a bifurcated cirri extending from posterior margin. Mouth terminal, upper lip broad, much wider in front of snout than on the sides. Upper jaw with 2+2 incisiform teeth anteriorly, followed by a single row of 10 small coniform teeth. Lower jaw with 2+2 incisiform teeth anteriorly, followed by single row of 6 coniform teeth. Diameter of eye 2.5 (2.5–3.1) and interorbital space 4.1 (3.4–5.4) in HL. Adhesive disc length 2.7 (2.5–2.7) and width 2.9 (2.8–3.3) in SL; 8 (7–9) transverse rows of papillae across width of disc region A; 10 (9–12) transverse rows of papillae across width of disc region B; 5–5 (3–5) longitudinal rows of papillae across width of disc region C. Pectoral length 4.8 (5.2–6.1) in SL. Pre-dorsal distance 1.4 (1.4–1.5). Dorsal length 5.7 (4.7–6.9). Caudal peduncle length 7.7 (5.9–10.4) and depth 11.0 (10.1–12.3) in SL.

TABLE 2 | Measurement comparisons among Acyrtus species. Data for A. simon and A. pauciradiatus were obtained in the present study. Data for A. artius, A. lanthanum, and A. rubiginosus were taken from Conway et al. (2014), and A. arturo from Tavera et al. (2021).

 

Acyrtus simon

A. pauciradiatus

A. artius

A. lanthanum

A. rubiginosus

A. arturo

Proportion in standard length

 

 

 

 

 

 

Head length

34–47

40–44

44–47

39–43

32–39

41–43

Head depth

19–21

18–2

14–18

15–18

13–16

19–27

Pelvic disc length

36–39

27–34

29–36

30–39

27–31

34–39

Pelvic disc width

30–36

32–36

29–34

31–38

22–30

31–32

Pre-dorsal distance

64–69

67–71

65–71

64–73

61–71

62–72

Pre-anal distance

70–75

69–76

67–78

71–77

66–80

70–76

Caudal Peduncle length

10–17

05–08

09–15

08–11

09–13

03–11

Caudal peduncle depth

08–10

10–11

07–10

09–14

07–09

07–09

Anus-Disk distance

06–12

12–13

08–15

04–08

12–14

13–18

Anus-anal fin distance

11–15

06–09

08–13

10–14

12–14

04–09

Proportion in head length

 

 

 

 

 

 

Snout length

20–33

09–15

20–27

22–30

26–32

10–15

Diameter eye

32–40

24–33

24–31

24–31

23–28

26–33

Interorbital

18–29

40–45

14–21

15–21

18–25

18–25

 

Color in alcohol. Body overall pale, with orange blotches and bands on the dorsal side and on the head; fins hyaline; pupils hyaline with black margin; orange blotches on the iris (Fig. 1).

Coloration in life. Based on color photographs of live specimens (Figs. 1–2): body with variable red and white bands covered by small red spots; white bands might present red blotches; bands wider anteriorly and narrowing towards the caudal fin; pupil rounded and black, with thin white margin; white and red stripes and bands radiating outward from pupil across iris; iris also with thin white margin; first one-third of pectoral fin red, the posterior part hyaline; dorsal fin over red band red, and over white band hyaline with small red spots; caudal fin with variable white and red bands.

Geographical distribution and habitat. Acyrtus simon is only known from Trindade Island, situated 1,160 km from the Brazilian coast. There are unconfirmed records for its presence in the Martin Vaz Archipelago (Guabiroba et al., 2020), which lies 40 km from Trindade. The species lives from intertidal habitat down to reefs 15 m depth (Fig. 2A). Acyrtus simon is commonly found taking shelter in cavities used by Diadema antillarum during the day (Fig. 2B), often sharing the protection from predators offered by spines with the Vitória-Trindade Chain (VTC) endemic Hypleurochilus brasil Pinheiro, Gasparini & Rangel, 2013, Apogon americanus Castelnau, 1855 and a number of others hosts.

FIGURE 2 | Acyrtus simon in the natural environment at Trindade Island. A. Photos taken during a night dive by J. L. Gasparini; and B. During the day by J-C. Joyeux.

Etymology. The specific name honors Thiony Emanuel Simon, our ichthyologist friend, who dedicated his career to study reef fishes, especially the fish biodiversity of the Vitória-Trindade Chain. To be treated as a noun in apposition.

Popular name. Thiony’s clingfish; Peixe-ventosa de Thiony.

TABLE 3 | Interspecific and intraspecific (blue boxes) divergence among species of Acyrtus, Arcos, and Gobiesox (percentage values – %).Acy sim: Acyrtus simon; Acy sp: Acyrtus sp; Acy pau: Acyrtus pauciradiatus; Acy aff arti: Acyrtus aff. artius; Acy arti: Acyrtus artius; Acy lan: Acyrtus lanthanum; Acy rub 1: Acyrtus rubiginosus lineage 1; Acy rub 2: Acyrtus rubiginosus lineage 2; Acy artu: Acyrtus arturo; Arc nud: Arcos nudus; Arc ery: Arcos erythrops; Gob pun: Gobiesox punctulatus; Gob rhe: Gobiesox rhessodon; Gob mae: Gobiesox maeandricus.

 

1

2

3

4

5

6

7

8

9

10

11

12

13

1. Acy sim

0.11

 

 

 

 

 

 

 

 

 

 

 

 

2. Acy sp

1.25

0.23

 

 

 

 

 

 

 

 

 

 

 

3. Acy pau

1.85

1.93

0.09

 

 

 

 

 

 

 

 

 

 

4. Acy aff arti

5.71

6.60

6.10

 

 

 

 

 

 

 

 

 

5. Acy arti

6.60

7.61

7.85

7.08

0.45

 

 

 

 

 

 

 

 

6. Acy lan

7.62

10.31

10.46

11.16

10.09

0.40

 

 

 

 

 

 

 

7. Acy artu

19.36

19.63

19.55

19.30

17.59

20.51

0.00

 

 

 

 

 

 

8. Acy rub 1

19.42

18.50

18.84

17.92

18.08

20.03

20.63

0.96

 

 

 

 

 

9. Acy rub 2

20

19.68

20.08

19.80

19.06

19.46

20.91

5.81

0.12

 

 

 

 

10. Arc nud

19.94

20.57

19.64

21.38

20.52

19.38

21.33

20.89

19.18

 

 

 

11. Arc ery

31.80

31.63

31.12

30.60

30.82

30.46

31.47

32.00

33.79

31.33

 

 

12. Gob pun

26.28

27.41

26.07

27.22

25.77

25.27

25.33

28.31

29.57

29.24

36.53

 

13. Gob mae

26.97

26.53

27.68

28.53

30.53

27.69

27.95

26.98

27.19

27.88

36.10

27.55

14. Gob rhe

28.35

28.62

29.89

29.22

28.93

28.41

28.64

28.42

27.86

27.56

37.69

29.57

18.55

 

Conservation status. Acyrtus simon is endemic of Trindade Island. Endemic fishes from this island have not been assessed by the International Union for Conservation Nature (IUCN, 2021), with the exception of Scartella poiti Rangel, Gasparini & Guimarães, 2004; it is considered Vulnerable (VU) due the possibility of habitat degradation associated with its limited distributional range. The latest Brazilian Red List (Portaria MMA Nº 148, de 7 de junho de 2022) considers several Trindade Island endemic species as VU (i.e., Halichoeres rubrovirens Rocha, Pinheiro & Gasparini, 2010, Malacoctenus brunoi Guimarães, Nunan & Gasparini, 2010, Stegastes trindadensis Gasparini, Moura & Sazima, 1999, and Sparisoma rocha Pinheiro, Gasparini & Sazima, 2010, but not S. poiti nor Elacatinus pridisi Guimarães, Gasparini & Rocha, 2004), possibly for the same reasons, and in addition to the risks of fishing and ornamental trade. Therefore, Acyrtus simon is recommended to be categorized as VU according to the IUCN categories and criteria (IUCN Standards and Petitions Subcommittee, 2019).

FIGURE 3 | Bayesian phylogeny of Acyrtus based on the COI gene. Bayesian posterior probability values are shown and the biogeographic province of lineages presented in the right. SWA: southwestern Atlantic; NWA: northwestern Atlantic; EP: eastern Pacific.

Phylogenetic analyses of Acyrtus. COI sequences of 573 bp were obtained for 73 individuals of 20 species. Our analyses suggest the northwestern Atlantic as the center of the diversification of Acyrtus, and show that the genus is composed by at least nine species, forming a non-monophyletic group of three major clades (Fig. 3). One clade is composed by Caribbean and Brazilian species, another clade by the Caribbean A. rubiginosus lineage 1, A. rubiginosus lineage 2 and Arcos nudus, and a third solely composed by A. arturo, from the tropical eastern Pacific. Although three species (A. artius, A. lanthanum and A. rubiginosus) present a high distributional overlap along most of the Caribbean, our analysis revealed two cryptic species supported by high values of posterior probability, Acyrtus aff. artius from Tobago Island, and Acyrtus aff. rubiginosus from Belize (Fig. 3). Three species are endemic to the Brazilian Province and form a monophyletic group, which has Acyrtus aff. artius as the closest related species (Fig. 3). Brazilian species present small distributions: Acyrtus simon is restricted to Trindade Island, A. pauciradiatus, is restricted to Fernando de Noronha Archipelago and Rocas Atoll, and the undescribed species (Acyrtus sp., Fig. 3) is only known from the Salvador region, on the northeastern Brazilian coast. In general, Caribbean species present higher interspecific divergence than Brazilian species (Tab. 3).

TABLE 4 | Divergence times (Mya) among Acyrtus species and Arcos nudus, and the 95% highest posterior density.

FIGURE 4 | Bayesian estimates of divergence time based on the mitochondrial COI gene. Posterior probability values reached 1–0.99 for all the main nodes (represented by the orange circle). The horizontal purple bars indicate 95% credibility intervals of node age estimation. The calibration nodes represent the divergence of the last common ancestors between (A) Pseudochromidae + Grammatidae + Gobiesocidae, (B) Grammatidae + Gobiesocidae, (F) all Gobiesocidae species, and (G) Acyrtus + Arcos + Gobiesox (see Conway et al., 2017).

The estimated date for the most recent common ancestor of the Atlantic species and A. arturo (eastern Atlantic) is at least 15 Mya, and the origin of Arcos nudus and the Acyrtus rubiginosus clade was among the oldest diversification events of the genus within the Atlantic (Fig. 4; Tab. 4). Most of the diversification in Acyrtus is recent, occurring during the Pliocene and Pleistocene. The Brazilian clade is the youngest, diversifying around 2.55 Mya, and the divergence time between Acyrtus simon and Acyrtus sp. is around 1.7 Mya (Fig. 4). Divergences were higher among Caribbean species than among Brazilian species.

TABLE 5 | FST index among Acyrtus in the Southwestern Atlantic. All values were significant (p<0.05).

FIGURE 5 | Haplotype network of Acyrtus artius and the representatives of Acyrtus in the southwestern Atlantic. FN = Fernando de Noronha.

Evolutionary history of Acyrtus simon. The close relationship between Acyrtus simon, from Trindade Island, and Acyrtus sp. from the Brazilian coast was also revealed in the haplotype network (Fig. 5) and through smaller FST values than Acyrtus pauciradiatus (Tab. 5). Acyrtus simon, represented by only three haplotypes (Fig. 5), presented low haplotype and nucleotide diversity (Hd = 0.362; π = 0.001). Neutrality tests presented negative values (Tab. 6), though the Skyline plot did not present evidence of recent population growth in Trindade Island (Fig. 6) due to the low number of haplotypes.

TABLE 6 | Diversity and neutrality indexes calculated for Acyrtus simon, Trindade Island.h = haplotypes number; Hd = haplotype diversity; SD Hd = standard deviation of Hd; π = nucleotide diversity; SD π = standard deviation of π.

FIGURE 6 | Bayesian skyline plot showing the effective population size fluctuation of Acyrtus simon through time (Mya) (black line: median estimation; purple: confidence interval).

Discussion​


Our study presents the first phylogeny of the genus Acyrtus including all known representatives, revealing: 1) insights on the evolutionary history of the genus; 2) the current paraphyletic status of the genus; 3) the Brazilian Province species complex as a monophyletic group; 4) and the presence of undescribed and cryptic species. Although our phylogenetic inference is based on a single DNA marker, our conclusions are based on high statistical support.

The absence of reliable fossil data for the family Gobiesocidae (but see Schwarzhans et al., 2017) constitutes as one of the main barriers to the understanding of its evolutionary history. The secondary calibration from the divergence times obtained by Near et al. (2013), and used by Conway et al. (2017), was used here to study the genus Acyrtus. Near et al. (2013) estimated the origin of the family Gobiesocidae in the Eocene, around 42.9 Mya, which is consistent with the emergence of most reef fish families, between 66 and 34 Mya (Bellwood, 2015). Around 39 Mya (Conway et al., 2017), shortly after the origin of the family Gobiesocidae, its New World lineage (subfamily Gobiesocinae) was formed during a period marked by great diversification in the Tethys Sea (Renema et al., 2008). It is possible that earlier Gobiesocidae lineages originated in the Tethys Sea and then colonized both the Atlantic/eastern Pacific and the Indian-western Pacific oceans (Floeter et al., 2008). However, earlier Gobiesocidae lineages could also have had their origins in any of the oceans, using the Tethys as a passage. For instance, Gobiosomatini (Gobiidae) (Thacker, 2015), also endemic of the new world, originated in a period similar to Gobiesocinae, likely via dispersal from the western Indian Ocean through the Tethys passage (Thacker, 2015). While little can be concluded about the center of origin of Gobiesocidae, it seems that the Tethys Sea was important for dispersal and early diversification in the family.

After the rise of the Gobiesocinae, Acyrtus lineagesand Arcos erythrops diverged much earlier than the closure of the Isthmus of Panama, around ~21 Mya. Therefore, this event did not influence the divergence between Gobiesocinae genera as commonly seen in other groups (Lessios, 2008). Tavera et al. (2021) found a similar divergence time for Arcos erythrops, although the placement of this species did not evidence the monophyly of Arcos and Acyrtus. Despite this, our results support the topology obtained by Conway et al. (2020) based on seven different genes. Nevertheless, further investigation of the Arcos phylogeny with broader taxon sampling is needed.

Our results also show the emergence of the western Atlantic Acyrtus at least 15 Mya (the age of the last common ancestor of Acyrtus + Arcos nudus) in a period of origin and diversification of most reef fish genera (Bellwood et al., 2015). Moreover, the origin of Acyrtus coincides with the emergence of the Amazon barrier, which could have prevented an earlier dispersal from the Caribbean to the Brazilian Province. It could explain the latter diversification of Acyrtus in the history of this genus (~3.9 Mya). In this case, the glacioeustatic sea-level changes of the Pleistocene/Pliocene could have contributed to the connectivity between regions, and to the crossing of the biogeographic barrier, as suggested for many other reef fishes (Rocha, 2003).

The diversification of the Brazilian complex of species started during the Pleistocene and these three species present restricted distributions: two are endemic to oceanic islands, and a third is only known from a narrow geographic range of the Brazilian northeastern coast. There are two hypotheses for speciation and colonization routes. The first involves the colonization of the Fernando de Noronha archipelago, with posterior colonization of the Brazilian coast, which recently colonized Trindade Island. This hypothesis is corroborated by the fact that a few Caribbean species are also found in Fernando de Noronha but not along the Brazilian coast (Rocha, 2003). This archipelago could be a gateway for Caribbean species to colonize Brazilian waters. A second hypothesis would involve the colonization of the Brazilian coast first, with a subsequent and earlier colonization of Fernando de Noronha, and a more recent colonization of Trindade also from the coast. Some reef fish lineages were more widely distributed along the southwestern Atlantic in the past, persisting as relicts in restricted locations (Rocha et al., 2010; Pinheiro et al., 2017). The exposure of seamounts during low sea-levels could have favored the colonization of the Vitória-Trindade Chain (Macieira et al., 2015; Pinheiro et al., 2017).

Even though we observed low genetic diversity in our results for A. simon, there was no sign of population bottlenecks or expansion in the neutrality test, differently from other VTC endemics (Pinheiro et al., 2017). Differently from species with wider distribution (Pinheiro et al., 2017), the restriction of Acyrtus to shallow reefs and its absence on the VTC seamounts may have constrained its connectivity between the coast and the islands and limited the input of new haplotypes. Recent population expansions are seen in many species along the western Atlantic (da Silva et al., 2015; Liedke et al., 2020) that seem to be related to a ~90% increase in reef area caused by the rise in sea-level following the last glacial maximum (Ludt, Rocha, 2015).

Both Conway et al. (2014) and our study show three undescribed Caribbean Acyrtus species, one of them closely related to Acyrtus artius and the two other to A. rubiginosus. The existence of many hidden lineages in the same genus may be attributed to the species small size, cryptic behavior, and a low morphological divergence. The latter, in particular, is commonly related to recent speciation and/or stabilizing selection on the ancestral phenotype (Milá et al., 2017). A similar pattern is found for Gouania (Gobiesocidae) in the Mediterranean Sea, where recent diversification and cryptic lineages were recognized by Wagner et al. (2019). These results evidence that future molecular studies for Gobiesocidae should lead to the discovery of many cryptic species. The most likely cause for the high diversification in this family (even within provinces) is related to their weak dispersal potential, small size, sedentary habit, and demersal eggs (Pires, Gibran, 2011). These life-history characteristics are among the most important drivers of speciation in the Brazilian Province (Pinheiro et al., 2018; Mazzei et al., 2021; Simon et al., 2021), and other taxonomic groups that share similar traits (e.g., Labrisomidae and Gobiidae) also show strong genetic structure and cryptic speciation within the Great Caribbean (Baldwin et al., 2011; Victor, 2014). Additionally, the distribution of the closely-related Brazilian Acyrtus species in different environments (mainland coast and oceanic islands) and localities with distinct levels of isolation suggests that ecological and peripatric speciation processes might be important drivers of diversification in Gobiesocidae (Rocha et al., 2005; Pinheiro et al., 2017; Simon et al., 2021).

Our phylogenetic inference discloses the paraphyletic nature of Acyrtus, which includes Arcos nudus in its clade. The first Acyrtus species (A. rubiginosus) was described in 1868, originally assigned to the genus Sicyases, a valid genus described based on Sicyases sanguineus Müller & Troschel, 1843. The genera Acyrtus and Arcos were described in the same article (Schultz, 1944), based on Acyrtus rubiginosus and Arcos erythrops, respectively. Arcos nudus was originally described by Linnaeus (1758) as Cyclopterus, a valid and now monotypic genus described based on Cyclopterus lumpus Linnaeus, 1758 (Cyclopteridae or lumpfishes). It was later reassigned as Gobiesox nudus by Briggs (1955), and afterwards as Arcos nudus by Fernholm, Wheeler (1983). All other Arcos species are from the tropical eastern Pacific and were originally described as Gobiesox, a valid genus described based on Gobiesox cephalus Lacépède, 1800.

Our phylogenetic analyses indicate that Arcos nudus should be reassigned to Acyrtus. This species shares several distinguishing morphological characters with other Acyrtus species, including large secretory cells present inside the groove present in the subopercular spine (Conway et al., 2014). Therefore, according to our data, the genus Arcos seems to be exclusive to the eastern Pacific, while most Acyrtus are found in the western Atlantic. Additional studies including more eastern Pacific Gobiesocidae species are necessary to better assess the status of Acyrtus arturo, from Malpelo Island (Tavera et al., 2021), and Arcos nudus, from the Atlantic, which could belong to other clades. Alternatively, a more complete phylogenetic analysis including all Arcos species could also show clades uniting Acyrtus and Arcos erythrops, suggesting the unification of Acyrtus and Arcos in a single genus. Finally, our results highlight that a broad sampling in Gobiesocidae family will bring important insights about evolutionary patterns of cryptobenthic fishes.

Comparative material examined. All from Brazil. Acyrtops beryllinus: CIUFES 2930, 3, 12.36–16.52 mm SL. CIUFES 130851, 1, 25.12 mm SL; Acyrtus pauciradiatus: CIUFES 2475, 1, 11.08 mm SL. CIUFES 2481, 2, 9.36–11.24 mm SL. CIUFES 2503, 1, 19.02 mm SL. CIUFES 2548, 1, 10.03 mm SL. Gobiesox barbatulus: CIUFES 307, 6, 20.26–47.64 mm SL. CIUFES 1368, 14, 40.77–57.50 mm SL. CIUFES 2923, 3, 34.30–49.72 mm SL. CIUFES 2883, 6, 13.14–30.47 mm SL. Tomicodon australis: CIUFES 130269, 2, 19.78–25.31 mm SL. CIUFES 130294, 2, 14.11–19.12 mm SL. CIUFES 130712, 1, 15.42 mm SL. CIUFES 130853, 13, 20.36–31.21 mm SL.

Acknowledgments​


We thank the Brazilian Navy for support during scientific expeditions to Trindade Island. We also thank Raphael M. Macieira, C. L. S. Sampaio, R. G. Santos for support in the field and with samples, Fabio Di Dario, Kevin W. Conway and Sergio R. Floeter for providing valuable literature. TLQ is supported by a FAPES doctoral fellowship (Fundação de Amparo à Pesquisa e Inovação do Espírito Santo), JLG by a CAPES doctoral fellowship (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and HTP by a FAPESP JP fellowship (Fundação de Amparo à Pesquisa do Estado de São Paulo; 2019/24215–2; 2021/07039–6). LAR and HTP are funded by the Hope for Reefs initiative of the California Academy of Sciences. We thank Michael M. Mincarone, Raphael M. Macieira, and an anonymous reviewer for their insightful and constructive comments on the various versions of our manuscript.

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Authors


Thais L. Quintão1, João Luiz Gasparini3, Jean-Christophe Joyeux2, Luiz A. Rocha4 and Hudson T. Pinheiro4,5

[1]    Programa de Pós Graduação em Biologia Animal, Dept de Ciências Biológicas, Universidade Federal do Espírito Santo, 29075-910 Vitória, ES, Brazil (TLQ) thaislquintao@hotmail.com.

[2]    Departamento de Oceanografia e Ecologia, Universidade Federal do Espírito Santo, 29075-910 Vitória, ES, Brazil. (JCJ) jean.joyeux@ufes.br.

[3]    Programa de Pós-Graduação em Ciências Ambientais e Conservação (PPG-CiAC), Instituto de Biodiversidade e Sustentabilidade, Universidade Federal do Rio de Janeiro (NUPEM-UFRJ), 27965-045 Macaé, RJ, Brazil. (JLG) gaspa.vix@gmail.com.

[4]    Department of Ichthyology, California Academy of Sciences, 94118 San Francisco, CA, USA. (LAR) Lrocha@calacademy.org.

[5]    Centro de Biologia Marinha, Universidade de São Paulo, 11600-000 São Sebastião, SP, Brazil. (HTP) htpinheiro@gmail.com (corresponding author).

Authors’ Contribution


Thais L. Quintão: Formal analysis, Investigation, Methodology, Visualization, Writing-original draft, Writing-review and editing.

João Luiz Gasparini: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Supervision, Writing-original draft, Writing-review and editing.

Jean-Christophe Joyeux: Data curation, Formal analysis, Investigation, Writing-review and editing.

Luiz A. Rocha: Investigation, Methodology, Validation, Writing-review and editing.

Hudson T. Pinheiro: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Supervision, Validation, Visualization, Writing-original draft, Writing-review and editing.

Ethical Statement​


Fish collection was authorized by the Brazilian Environmental Agency, Instituto Chico Mendes de Conservação da Biodiversidade (SISBIO 12786–1 and 20880–2), and was in accordance with the ethical principles for animal experimentation, approved by the Ethics Committee for the Use of Animals of the Universidade Federal do Espírito Santo (CEUA-UFES 017–2009).

Competing Interests


The authors declare no competing interests.

How to cite this article

Quintão TL, Gasparini JL, Joyeux J-C, Rocha LA, Pinheiro HT. Recent dispersal and diversification within the clingfish genus Acyrtus (Actinopterygii: Gobiesocidae), with the description of a new western Atlantic species. Neotrop Ichthyol. 2022; 20(3):e210137. https://doi.org/10.1590/1982-0224-2021-0137


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© 2022 The Authors.

Diversity and Distributions Published by SBI

Accepted May 30, 2022 by Michael Mincarone

Submitted September 19, 2021

Epub October 03, 2022