Research Article |
Corresponding author: Hossein Ashrafi ( ashrafi.hossein.s@gmail.com ) Academic editor: Martin Schwentner
© 2023 Hossein Ashrafi, Kristin M. Hultgren.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Abstract
The alpheid snapping shrimp genus Synalpheus Spence Bate, 1888, is a prominent component of arthropod diversity found in coral reefs. Notably, Synalpheus is the only genus of marine organisms known to exhibit eusocial behavior. Although eusociality has evolved at least four times independently in Synalpheus, all described eusocial species are from the West Atlantic, with only a single study documenting possibly eusocial species from Indonesia. In 2008, during an expedition to Madagascar organized by the Florida Museum of Natural History (
Synalpheus, phylogeny, sponge-dwelling, Madagascar, new species, S. gustavi sp. nov., S. sponjy sp. nov.
The snapping shrimp in the genus Synalpheus Spence Bate, 1888, comprise a major component of the crustacean diversity within coral reefs (
Extensive research has delved into various aspects of this unique lifestyle, encompassing colony composition (
In 2008, a comprehensive expedition to Madagascar was organized by the Florida Museum of Natural History (
Notably, the expedition to Madagascar yielded a significant number of cryptic sponges, which were frequently sampled. This fortuitous circumstance provided an ample opportunity to study the Synalpheus species associated with these sponges. Among the inhabitants of the sponges, two distinct species of Synalpheus stood out, with each species represented by a substantial number of specimens collected from a single sponge. Interestingly, within each sponge, only a single ovigerous female was found, if any.
By conducting a meticulous examination of both species, it became evident that they had developed a eusocial living system, marking a remarkable discovery previously undocumented in the Western Indian Ocean. These two previously unknown species are now being formally described and have been incorporated into a multi-gene phylogenetic tree. This inclusion allows for the reconstruction of how many times eusociality has independently evolved outside of the Western Atlantic Synalpheus species.
The materials for the present study were collected during several expeditions conducted by the Florida Museum of Natural History (
The most recent comprehensive worldwide tree of Synalpheus (
All species sequenced for phylogenetic analyses used in this study, including the genetics # (referenced in phylogenetic trees), locality, collection number, and GenBank accession numbers. For the complete list of the abbreviations used in the voucher numbers, see Supplementary data 1 in
Species | Genetics# | Locality | Collection# | COI | PEPCK | 16S | 18S |
---|---|---|---|---|---|---|---|
Synalpheus africanus | 592 | São Tomé | AA--06-215 | KJ595031 | KJ625140 | KJ625020 | |
Synalpheus cf. africanus B | 595 | Sao Tome | OUMNH.ZC.2012-07-130 | KJ595053 | KJ625142 | KJ595185 | KJ595255 |
Synalpheus agelas | 459 | Belize | CBC09-1508 | KJ595032 | HQ435419 | KJ595245 | |
Synalpheus anceps | 2182 | Guam |
|
OR482981 | OR483005 | OR483030 | |
Synalpheus androsi | 467 | Belize | CBC09-6502 | KJ625033 | HQ435421 | KJ595246 | |
Synalpheus ankeri | 477 | Panama | P09-6903 | KJ625041 | KJ625069 | HQ435473 | KJ595242 |
Synalpheus apioceros | 593 | Panama | RMNH.CRUST.D.54889 | KJ595035 | KJ625141 | KJ595177 | KJ595247 |
Synalpheus bannerorum | 563, 634 | Panama | OUMNH.ZC.2014-04-027 | KJ595036 | KJ595178 | ||
Synalpheus belizensis | 250 | Barbados | BR08-6901 | KJ595038 | KU682627 | ||
Synalpheus bituberculatus | 1290 | Singapore | OUMNH.ZC.2014-11-190 | OR482983 | OR483007 | OR483032 | |
Synalpheus bituberculatus | 1291 | Singapore | OUMNH.ZC.2014-11-190 | OR482982 | OR483006 | OR483031 | |
Synalpheus bocas | 16 | Jamaica | JAM08-7402 | KJ595041 | KJ625107 | HQ435426 | KJ595249 |
Synalpheus bousfieldi | 483 | Belize | CBC09-3605 | KJ595042 | KJ625073 | KJ595250 | |
Synalpheus brevifrons | 481 | Belize | CBC09-2704 | KJ625034 | KJ625072 | HQ435435 | KJ595251 |
Synalpheus brooksi | 476 | Panama | P09-3102 | KJ595049 | KJ625068 | HQ435437 | KJ595253 |
Synalpheus brooksi | 479 | Panama | P09-4911 | KJ625035 | KJ625070 | HQ435438 | KJ595252 |
Synalpheus carpenteri | 421 | Jamaica | JAM08-3008 | KJ595052 | HQ435439 | KU682628 | |
Synalpheus cayoneptunus | 910 | Florida | VIMS 13FK2901, 2903 | KM204166 | KM204180 | KU682629 | |
Synalpheus chacei | 457 | Belize | CBC09-501 | KJ595059 | KJ625062 | HQ435440 | KJ595265 |
Synalpheus chaki | 2014_1228 | Martinique | MNHN-IU-2014-1228 | MZ323456 | MZ329362 | ||
Synalpheus charon A | 565 | Egypt | OUMNH.ZC.2014-02-022 | KJ595060 | KJ625128 | KJ595191 | KJ595266 |
Synalpheus charon C | 566 | Taiwan |
|
KJ595064 | KJ595192 | KJ595269 | |
Synalpheus corallinus | 826 | Jamaica | JAM12-9902 | KU980212 | HQ435441 | KU682630 | |
Synalpheus corbariae | 2014-1238 | Martinique | MNHN-IU-2014-1238 | MZ323450 | MZ329367 | ||
Synalpheus coutierei B | 2164 | French Polynesia |
|
OR482984 | OR483008 | OR483033 | |
Synalpheus dardeaui | 461 | Belize | CBC09-3105 | KJ625036 | KJ625110 | HQ435442 | KJ595271 |
Synalpheus dominicensis | 482 | Belize | CBC09-2906 | KJ477702 | KJ494390 | KJ477695 | KU682632 |
Synalpheus duffyi | 26 | Jamaica | JAM08-7403 (26), VIMS 08JAM7401-2 | KJ595078 | HQ435444 | KU682633 | |
Synalpheus elizabethae | 944, 137 | Panama | P08-12504 (137) | KU980213 | HQ435446 | KU682634 | |
Synalpheus filidigitus | 470 | Belize | CBC09-7603 | KJ595079 | KJ625066 | HQ435447 | KJ595275 |
Synalpheus fossor | 570 | Thailand | OUMNH.ZC.2011-03-096 | KJ595080 | KJ595199 | KJ595276 | |
Synalpheus goodei | 464 | Belize | CBC09-5404 | KJ477698 | KJ625065 | HQ435448 | KJ595279 |
Synalpheus guerini A | 527, 541 | Florida |
|
KJ595082 | KJ595200 | KJ595282 | |
Synalpheus gustavi n. sp. | 707 | Madagascar |
|
KJ494394 | |||
Synalpheus gustavi n. sp. | 2172 | Madagascar |
|
OR482985 | OR483010 | ||
Synalpheus gustavi n. sp. | 2173 | Madagascar |
|
OR482986 | OR483011 | ||
Synalpheus gustavi n. sp. | 2175 | Madagascar |
|
OR482987 | OR483012 | ||
Synalpheus gustavi n. sp. | 2184 | Madagascar |
|
OR483009 | |||
Synalpheus gustavi n. sp. | 2180 | Madagascar |
|
OR483013 | |||
Synalpheus hastilicrassus A | Syn2119 | Queensland |
|
OR482988 | OR483015 | ||
Synalpheus hastilicrassus A | 678 | Queensland |
|
KJ625055 | KJ625098 | KJ595284 | |
Synalpheus hastilicrassus B | 596 | Queensland |
|
KJ595089 | KJ625143 | KJ595206 | KJ595287 |
Synalpheus hastilicrassus C | Syn2111 | Hong Kong |
|
OR482989 | KJ625134 | OR483016 | KJ595288 |
Synalpheus hastilicrassus_D | Syn2109 | Guam |
|
OR482990 | OR483017 | ||
Synalpheus hastilicrassus_F | Syn2118 | Queensland |
|
KJ625061 | KJ625134 | OR483014 | KJ595288 |
Synalpheus hemphilli | 571 | Florida |
|
KJ595092 | KJ595208 | KJ595290 | |
Synalpheus herricki | 157 | Curacao | CU08-3202 | KJ595095 | HQ435449 | KU682635 | |
Synalpheus hoetjesi | 202 | Curacao | CU08-2901 | KJ625037 | KJ625076 | HQ435452 | KJ595293 |
Synalpheus idios | 474 | Belize | CBC09-8803 | KJ625038 | KJ625115 | HQ435455 | |
Synalpheus iocasta | 1284 | Singapore | OUMNH.ZC.2014-11-219 | OR482991 | OR483018 | OR483034 | |
Synalpheus irie | 38, 493 | Jamaica | JAM08-3601 | KJ595106 | KJ625117 | HQ435457 | KJ595294 |
Synalpheus kensleyi | 504 | Panama | P07-1204 | KJ625039 | KJ625119 | HQ435458 | KJ595295 |
Synalpheus kuadramanus | 843 | Jamaica | VIMS 12JAM9501 | KU980214 | MZ329378 | KU682637 | |
Synalpheus lani | 599 | Panama | OUMNH.ZC.2014-04-030 | KJ595107 | KJ625145 | KJ595210 | KJ595296 |
Synalpheus aff. longicarpus | 488 | Panama | P09-9101 | KJ595025 | KJ625075 | HQ435459 | KJ595240 |
Synalpheus macdonaldi | 2014_1227 | Martinique | MNHN-IU-2014-1227 | MZ323448 | MZ329364 | ||
Synalpheus mcclendoni | 237 | Barbados | BR08-1413 | KJ595109 | HQ435462 | KU682639 | |
Synalpheus microneptunus | 247 | Barbados | BR08-6001 | KJ595110 | KJ625108 | HQ435463 | KU682640 |
Synalpheus aff. sanctithomae | 471 | Belize | CBC09-7804 | KJ625043 | KJ625114 | HQ435464 | KJ595243 |
Synalpheus aff. sanctithomae | 486 | Belize | CBC09-8701 | KJ595029 | KJ625074 | HQ435465 | KJ595244 |
Synalpheus neomeris_A | 1133 | Saudi Arabia |
|
OR482992 | OR483019 | OR483035 | |
Synalpheus neomeris_A | 573 | Madagascar |
|
KJ595056 | KJ595188 | KJ595260 | |
Synalpheus neptunus A | 560 | Queensland |
|
KJ595119 | KJ625126 | KJ595217 | |
Synalpheus neptunus B | 1119 | Queensland |
|
OR482994 | OR483021 | ||
Synalpheus cf. neptunus germanus | 1117 | Western Australia |
|
OR482993 | OR483020 | OR483036 | |
Synalpheus nobilii | 576 | Panama | OUMNH.ZC.2013-03-009 | KJ595122 | KJ625132 | KJ595219 | KJ595303 |
Synalpheus obtusifrons | 465 | Belize | CBC09-6303 | KJ477703 | KJ494389 | HQ435466 | KJ494396 |
Synalpheus pandionis | 472 | Belize | CBC09-8403 | KJ595126 | KJ625067 | HQ435468 | KJ595305 |
Synalpheus parfaiti | 609 | Sao Tome | MNHN-IU-2010-4150 | KJ595127 | KJ595223 | ||
Synalpheus pectiniger | 500 | Jamaica | JAM08--8801 | KJ595129 | KJ625118 | HQ435470 | KJ595307 |
Synalpheus peruvianus | 601 | Panama | OUMNH.ZC.2013-03-056 | KJ595132 | KJ625147 | KJ595224 | KJ595310 |
Synalpheus plumosetosus | 231 | Jamaica | JAM08-2704 | KU980220 | HQ435471 | ||
Synalpheus rathbunae | 941 | Panama | P08--3501-2 | KU980221 | AY344767 | KU682644 | |
Synalpheus regalis | 469 | Belize | CBC09-7002 | KJ625042 | KJ625113 | HQ435474 | |
Synalpheus ruetzleri | 466 | Belize | CBC09-6201 | KJ595136 | KJ625112 | HQ435475 | KJ595313 |
Synalpheus sanctithomae | 235 | Barbados | BR08-1201 | KJ595139 | AY344768 | KU682647 | |
Synalpheus sanlucasi | 654 | Panama | OUMNH.ZC.2013-03-015 | KJ625049 | KJ625089 | KJ595225 | KJ595317 |
Synalpheus scaphoceris | 683 | Panama | MNHN-IU-2010-4152 | KJ625058 | KJ595226 | KJ595318 | |
Synalpheus sladeni | 1137 | Madagascar |
|
OR482995 | OR483022 | OR483037 | |
Synalpheus somalia aff. | 2186 | Saudi Arabia |
|
OR482996 | OR483023 | OR483038 | |
Synalpheus spinifrons | 611 | Chile | AA--07-317 | KJ595145 | KJ595228 | KJ595321 | |
Synalpheus sponjy n. sp. | 2178 | Madagascar |
|
OR482998 | OR483025 | OR483039 | |
Synalpheus sponjy n. sp. | 2176 | Madagascar |
|
OR482997 | OR483024 | ||
Synalpheus sponjy n. sp. | 2179 | Madagascar |
|
OR482999 | OR483026 | ||
Synalpheus stimpsonii_A | 553 | Queensland |
|
KJ595147 | KJ595229 | KJ595323 | |
Synalpheus stimpsonii_B | 554 | Queensland |
|
KJ595148 | KJ595230 | KJ595325 | |
Synalpheus stimpsonii_C | 1109 | Queensland |
|
OR483000 | OR483027 | KJ595326 | |
Synalpheus streptodactylus A | 584 | Madagascar |
|
KJ595151 | KJ595234 | KJ595327 | |
Synalpheus thai | 1281 | Singapore | OUMNH.ZC.2014-11-263 | OR483001 | OR483028 | OR483040 | |
Synalpheus theano | 1286 | Singapore | OUMNH.ZC.2014-11-266 | OR483002 | OR483029 | OR483041 | |
Synalpheus theano | 1285 | Singapore | OUMNH.ZC.2014-11-264 | OR483003 | |||
Synalpheus theano | 2183 | Western Australia |
|
OR483004 | |||
Synalpheus thele | 113 | Jamaica | JAM08-8924 | KJ595156 | KJ625106 | KJ595335 | |
Synalpheus ul | 253 | Barbados | BR08-8703 | KJ625044 | KJ625109 | HQ435482 | KU682648 |
Synalpheus williamsi | 462 | Belize | CBC09-5102 | KU980224 | KJ625064 | HQ435484 | KJ595338 |
Synalpheus yano | 484 | Belize | CBC09-3802 | KJ595161 | KJ625116 | HQ435485 | KJ595339 |
Alpheus percyi (outgroup) | 0 |
|
KJ477697 | KJ494392 | KJ477694 | KJ494395 |
Tissue from the gills, eggs, and/or pleopods 3-5 were used for genomic DNA extraction using the QIAGEN DNeasy Blood and Tissue kit, following standard manufacturer protocols. We amplified the COI and 16S loci using PCR and thermocycler conditions described in
Forward and reverse sequences were cleaned, aligned, and translated to amino acids to check for stop codons using Sequencher (Gene Codes, Ann Arbor, MI, USA) and MEGA v. 11 (
CL – Carapace length;
The consensus phylogenetic tree constructed in this study (Fig.
Phylogenetic tree constructed for the members of the genus Synalpheus using the Bayesian Inference approach based on a concatenation of four genes: 16S, COI, PEPCK, and 18S. Bayesian posterior probabilities are provided above each branch. Taxa are shown as Synalpheus species plus unique identifier (see supplementary table S1). Eusocial species are indicated with an arrow (red, WA= West Atlantic; blue, IWP = Indo-West Pacific).
The results of the phylogenetic study using Bayesian inference (Fig.
The previously recognized S. gambarelloides group is no longer a monophyletic clade (possibly due to the lack of morphological characters). Several of its members are now positioned outside the traditional S. gambarelloides clade. Synalpheus rathbunae Coutière, 1909, group; S. paraneptunus Coutière, 1909, group; S. herricki Coutière, 1909; S. pectiniger Coutière, 1907; S. androsi Coutière, 1909; S. kensleyi (
In the current phylogenetic study, we identify seven distinct lineages of eusociality: the entire S. rathbunae clade; appearing multiple times within the S. paraneptunus clade; within S. brooksi Coutière, 1909, species complex; as well as involving S. chacei; S. gustavi sp. nov.; S. sponjy sp. nov.; and at least two occurrences within the S. neptunus species complex. While S. crosnieri is not encompassed within the phylogenetic analysis, it is undoubtedly closely related to S. sponjy sp. nov. owing to numerous morphological similarities between the two species. Moreover, it is noteworthy that S. paradoxus might potentially introduce a new lineage of eusociality within the genus.
The COI Bayesian gene tree (Fig. S1) indicated that multiple sequenced specimens of the two new species are reciprocally monophyletic, with Bayesian posterior probabilities = 1.
Infraorder Caridea Dana, 1852
Family Alpheidae Rafinesque, 1815
Genus Synalpheus Spence Bate, 1888
The new species derives its name from the Malagasy word ‘sponjy’, which translates to ‘sponge’. The term is used as a noun in opposition.
Holotype
: MADAGASCAR • 1 male (CL 3.6 mm); Nosy Be; 13°25’9.7”S, 48°15’37.94”E; 17 May 2008; Bakary G, Bruggermann H, Michonneau F, Paulay G, Werner T leg.; 6-9 m, from cryptic sponge;
Small-sized species of Synalpheus. Carapace (Fig.
Male pleon (Fig.
Telson (Fig.
Antennula (Fig.
Antenna (Fig.
Mouthparts not dissected. Third maxilliped (Fig.
Major cheliped (Fig.
Second pereiopod (Fig.
Third pereiopod (Fig.
Uropods (Fig.
North of Madagascar: Nosy Be and Nosy Vorona.
All the specimens were collected from cryptic sponges situated among dead coral and coral rubbles.
The new species exhibits similarities to several rare species found in the Indo-West Pacific region, characterized by a dense brush of setae on the dactylus of the minor cheliped, known as gambarelloides setae. These species include S. sladeni Coutière, 1908; S. spongicola Banner and Banner, 1981; S. crosnieri Banner and Banner, 1983; and S. gambarelloides (Nardo, 1847) [as reported in
According to
Synalpheus sponjy sp. nov. is closely related to the other two species, S. crosnieri and S. spongicola, both of which have not been reported since their original descriptions. The new species can be distinguished from S. crosnieri (found northwest of Madagascar) by the overall shape of the major cheliped fingers. In S. sponjy sp. nov., the major cheliped is normal and straight, whereas in S. crosnieri, it appears twisted when viewed dorsally. Additionally, the shape of the meri in the third and fourth pereiopods sets the new species apart. In the new species, these meri are concave on the distal half, and the third pereiopod merus bears a row of stiff setae along the mesial margin of the concavity. However, caution should be exercised when using the latter characteristic as the drawings provided by
One of the authors (HA) had the opportunity to examine the type series of S. spongicola deposited in the Naturalis Biodiversity Center, Leiden, Netherlands. As mentioned by
In the phylogenetic tree (Fig.
Synalpheus aff. brevifrons Hultgren, Hurt and Anker, 2014; Ashrafi and Hultgren, 2022.
The new species is named after Gustav Paulay (
Holotype
: MADAGASCAR • 1 male (CL 3.4 mm); Nosy Vorona; 15 May 2008; Paulay G leg.; 4m, in cryptic sponge;
Small-sized species of Synalpheus. Carapace (Fig.
Pleon only showing sexual dimorphism in first pleonite. Male pleon (Fig.
Telson (Fig.
Antennula (Fig.
Antenna (Fig.
Mouthparts not dissected. Third maxilliped (Fig.
Major cheliped (Fig.
Second pereiopod (Fig.
Three last pereiopods (Fig.
Uropods (Fig.
North of Madagascar: Nosy Vorona.
All the specimens were collected from cryptic sponges situated among dead coral and coral rubble.
The new species, S. gustavi sp. nov., shares a distinctive spoon-shaped feature of the minor cheliped, along with the presence of an orbitorostral process, with several species found in the Indo-Pacific region. These species include S. anceps AH Banner, 1956; S. dorae
The new species can be distinguished from the aforementioned species based on four distinct characteristics, allowing for a quick and accurate differentiation. These traits are as follows: 1) very shallow frontal margin of the carapace, both the rostrum and orbital teeth, 2) unique shape of the ultimate segment of the third maxilliped, 3) presence of a four-articled carpus in the second pereiopod, and 4) exceptionally narrow and slender fingers in the second pereiopod.
Synalpheus anceps, which was reported from Saipan in the Northern Mariana Islands (AH
Synalpheus dorae shares one of the four distinctive characteristics of S. gustavi sp. nov., i.e. the second pereiopod with four-articled carpus. However, there are several other notable differences between the new species and S. dorae: the less developed superior tooth of the basicerite in the new species compared to that of S. dorae, the more developed scaphocerite blade in S. dorae, the major chela palm terminating to a small projection dorso-distally in S. gustavi sp. nov. while bearing a prominent tooth in S. dorae, more robust three last pereiopods with dorsal ungui about three times as long as ventral ungui in S. gustavi sp. nov. compared to slightly longer superior ungui in S. dorae, very strong dorsal spiniform setae of telson, and very narrow posterior margin of telson in S. dorae with mesial spiniform setae being juxtaposed.
Three species, namely S. harpagatrus, S. laticeps, and S. paralaticeps, are distinguished by the specific shape of the fingers on the minor cheliped, which possess 3 or 4 teeth at the tip. In contrast, the new species has a single tooth and a tiny accessory tooth on the fingers. Additionally, the following differences, in addition to the four main distinctions, can be observed between these three species and the new species: the longer stylocerite (overreaching the first antennular article) and more developed blade of the scaphocerite in the three of them compared to S. gustavi sp. nov.; typical ultimate segment of the third maxilliped in S. laticeps and S. paralaticeps compared to broad distally and armed with 13 slender spiniform setae in S. gustavi sp. nov., and narrow distally armed with 10-12 short heavy spiniform setae in S. harpagatrus; stouter general shape of the minor cheliped in S. harpagatrus; armed merus of the third pereiopod in S. harpagatrus and S. paralaticeps but unarmed in S. laticeps and S. gustavi sp. nov.; proportion of the superior unguis of the third pereiopod dactylus to the inferior one being approximately 3 in S. gustavi sp. nov., 2 in S. paralaticeps and 1 in S. harpagatrus and S. latirostris; fully developed diaeresis in S. harpagatrus and S. paralaticeps compared to the reduced one to a lateral tooth in S. gustavi sp. nov.; straight posterior margin of the telson in S. gustavi sp. nov. compared to the convex one in the other three species.
The Red Sea-inhabiting species, S. paradoxus, can be further distinguished from S. gustavi sp. nov. by the following characteristics, in addition to the four previously mentioned differences: its very strong superior tooth of the basicerite; half-developed blade of the scaphocerite; major cheliped merus armed with a strong tooth dorso-distally, palm with strong tubercle on the dorso-distal margin, and the dactylus longer than the pollex; minor cheliped dactylus with two definite rows of setae situated dorsally and mesially; third pereiopod dactylus with the superior unguis about twice as long as the inferior unguis; complete diaeresis; and triangular distolateral angles of the telson.
The three remaining species S. neptunus neptunus, S. neptunus germanus and S. theano, are separable from the new species by various characters, in addition to the four mentioned differences (
Phylogenetically speaking, S. gustavi sp. nov. was initially included in the first and only worldwide phylogenetic study of the genus Synalpheus (
Since the initial documentation of eusociality in Synalpheus shrimps, prerequisites for the evolution of eusociality, as well as numerous distinctive characteristics unique to eusocial species have been reported and extensively discussed (for instance,
One of the most remarkable examples of division of labor was observed by Duffy (1999) in larger females of S. filidigitus Armstrong, 1949. While smaller females maintain a morphology similar to other colony members, the larger females were reported to lack the massive major cheliped (their defensive tool) and instead rely on two minor chelipeds (their feeding tools), representing a striking transition towards division of labor. Interestingly, the first observation of females with two minor chelipeds in the Indo-Pacific species of Synalpheus was documented by
Synalpheus sponjy sp. nov. not only represents the species that is morphologically closest to S. crosnieri but also exhibits a similar life style. While no females were found in the collected colonies of the new species, the assemblages of the collected specimens within a sponge varied between 1 and 19 males. Like other eusocial species of Synalpheus, this species inhabits cryptic sponges situated among dead corals, making it challenging to sample the entire sponge (and the entire colony) during a typical survey of coral rubble. However, considering the number of collected specimens (24 males), and the fact that 19 of them were collected from a single sponge, the most likely conclusion is that S. sponjy sp. nov., like its sister taxon, is a eusocial species.
In contrast to the rarity of the gambarelloides small chela type in Indo-Pacific species, the prevalence of the spoon-shaped type of chela is notable in this region, with several species showing indications of evolving a eusocial system. One such species is S. neptunus germanus, described by Banner and Banner in 1975 based on 44 specimens collected from three different sites. Although all specimens were reported as juveniles, there are indications that the species is eusocial based on personal observations of the authors. Furthermore, eusociality has been observed in at least one additional species within the S. neptunus group.
Lastly, the newly discovered species, S. gustavi sp. nov., represents another eusocial species characterized by the spoon-shaped fingers of the small chela. Alongside the number and size of eggs, S. gustavi sp. nov. exhibits one of the most significant hallmarks of eusociality—a skewed sex ratio. Colony sizes ranged from 1 to 19 individuals, although it is possible that some records of solitary individuals originated from individuals separated from the rest of their colonies within the rubble. Among colonies with females, the sex ratio varied from 1/3 (UF 14231) to 1/19 (UF 14259, including the allotype ovigerous queen). Interestingly, colonies of S. gustavi sp. nov. showed a tendency for high rates of parasitism (primarily in the pleonal area) by bopyrid isopod parasites. The rates of individual lot parasitism ranged from 0% to 50% (mean = 14.4%), comparable to the parasitism rates reported in some eusocial Synalpheus colonies by Duffy (1992) (30% in S. brooksi) and (McGrew and Hultgren, 2011) (25% in S. elizabethae).
In summary, the two new species, S. sponjy sp. nov. and S. gustavi sp. nov., exhibit assemblages indicative of a eusocial colony structure. These include the presence of large numbers of male (non-ovigerous) individuals residing together in a single sponge, with one or zero females present. Additionally, the two new species share ecological and morphological characteristics with other described eusocial Synalpheus species. Firstly, both species inhabit sponges, a symbiotic lifestyle believed to be a prerequisite for the evolution of eusociality. Moreover, the presence of multiple size classes, including juveniles, within the same sponge suggests overlapping generations, further supporting their eusocial nature. Secondly, similar to eusocial species in the West Atlantic, the two new species are relatively small-bodied (mean CL of S. gustavi sp. nov. = 2.62, mean CL of S. sponjy sp. nov. = 2.93), comparable to the body size of other described eusocial species (mean = 3.2 mm CL), but smaller than the average body size of communal species (mean CL = 5.32) and pair-living species (mean CL = 5.57) (
Eusociality has been extensively documented and studied in several Atlantic species of Synalpheus. However, numerous Indo-West Pacific species of Synalpheus with a high likelihood of possessing a eusocial living style have remained unnoticed, as they were described and/or reported prior to 1996 when eusociality was first reported in Synalpheus by Duffy in 1996.
The recent descriptions of two new species and the presence of at least four other eusocial species in the Indo-West Pacific region emphasize the likelihood of multiple independent evolutions of eusociality within the genus Synalpheus. These findings highlight the importance of conducting taxonomic and ecological studies on species within this region.
It is important to acknowledge the significant contributions made by Coutière, De Man, and Banner and Banner in their work before 1986, which greatly enhanced our understanding of Synalpheus species in the Indo-West Pacific. However, it is evident that earlier studies did not emphasize eusocial behavior and overall living styles, primarily due to the lack of recognition of eusociality before Duffy’s publication in 1996. The limited taxonomic and ecological studies on Indo-West Pacific species of the genus indicate a noticeable gap in our understanding. The species richness of Indo-West Pacific Synalpheus, particularly in terms of eusocial species, is currently underestimated. Therefore, it is crucial to conduct further research and observations to deepen our understanding of the taxonomy, morphology, and ecology of this fascinating genus. Continued research efforts will undoubtedly illuminate the complex behaviors, social structures, and ecological interactions of Synalpheus species not only in the Indo-West Pacific region but also in other regions, especially poorly-studied ones such as the East Pacific. Ultimately, this will lead to a more comprehensive understanding of this remarkable group of organisms.
HA: Conceptualization, Methodology, Original draft.
KH: Conceptualization, Methodology, Review and Editing.
The study was financially supported by the student grant project SGS01/PřF/2023 (to HA).
The author has declared that no competing interests exist.
All the sequences used in the study are submitted to the GenBank with the numbers provided in the Table
We are sincerely grateful for the invaluable insights, comments, and recommendations generously provided by our esteemed reviewers, Charles H.J.M. Fransen and Sammy De Grave. The specimens used in this study were collected during the
Fig. S1
Data type: .tif
Explanation note: Bayesian gene tree based on COI sequences. Numbers above clades indicate Bayesian posterior probabilities. Taxon labels are given as Synalpheus species, locality, and genetics identifier (given in Table S1). New species described in this study are figured in red.