Sexual dimorphism is known in fossils of many invertebrate groups (Westerman Reference Westerman1969, Reference Westermann1979). It is recognised almost exclusively in their preserved mineralised hard parts (shell, carapace), in overall size differences and/or a range of other, group-specific morphological features. For example, in molluscs it has been extensively reported from Mesozoic cephalopods (e.g., Calloman Reference Callomon1963, Reference Callomon, House and Senior1980; Lehmann Reference Lehmann1981), and it is also recognised in Miocene gastropods (Halder & Paira Reference Halder and Paira2019) and a Jurassic bivalve (Karapunar et al. Reference Karapunar, Werner, Fürsich and Nützel2021). Additionally, the tests of a few Cretaceous and Cenozoic echinoids display dimorphism (Philip & Foster Reference Philip and Foster1971; Néraudeau Reference Néraudeau1993).
There are many examples of sexual dimorphism within fossil arthropods. Various trilobite species have been claimed to be sexually dimorphic, based for example on differences in size or the eye (Clarkson Reference Clarkson and Westerman1969; Hu Reference Hu1971), but most such examples have been regarded as unrigorously supported (Hughes & Fortey Reference Hughes, Fortey, Cooper, Droser and Finney1995; Fortey & Hughes Reference Fortey and Hughes1998). However, more likely instances include those which show the presence/lack of a preglabellar brood pouch in Cambrian and Ordovician species (Fortey & Hughes Reference Fortey and Hughes1998; see also Cederström et al. Reference Cederström, Ahlberg, Nilsson, Ahlgrens and Eriksson2011) or of an anterior median spine in raphiophorids (Knell & Fortey Reference Knell and Fortey2005) or of a long trident-like anterior cephalic projection in the asteropygine Walliserops (Gishlick & Fortey Reference Gishlick and Fortey2023). In chelicerates sexual dimorphism has been proposed in a Silurian pycnogonid (Siveter et al. Reference Siveter, Sabroux, Briggs, Siveter and Sutton2023), where the female form displays a thickened trunk and coxa (related to the possession of ovaries and egg development); male eurypterids have been identified on the grounds of supposed sperm-carrying parts (Kamenz et al. Reference Kamenz, Staude and Dunlop2011); and a Xiphosuran specimen has been designated as male based on its anterior scalloped carapace margin (Lamsdell & McKenzie Reference Lamsdell and McKenzie2015). Instances of sexual dimorphism in non-ostracod crustaceans include Jurassic lobsters (Chény et al. Reference Chény, Charbonnier and Audo2023) and insects, for example in a Cretaceous beetle (Jiang et al. Reference Jiang, Liu and Wang2019).
Ostracod crustaceans are known from at least 33,000 living and fossil species (Horne et al. Reference Horne, Cohen, Martens, Holmes and Chivas2002) and arguably are by far the most specimen abundant group of arthropods in the fossil record. Shell dimorphism is common in all the major ostracod taxa but is most glaring in several major Palaeozoic groups. Beyrichioidean (Palaeocopida) ostracods, known abundantly worldwide from hundreds of genera, from the Ordovician to the Carboniferous, are characterised by well-defined shell dimorphism. Herein we report a commonly occurring Silurian beyrichioidean ostracod species from the UK that is unique in seemingly being non-dimorphic, thereby challenging the definition of the group. Reasons for its possible non-dimorphic nature include heterochronic mechanisms. Seemingly not all beyrichioideans had the same brood care strategy.
1. Ontogeny and dimorphism in ostracods
Ostracods grow by ecdysis (Fig. 1), when the cuticle is shed and a new, larger one is secreted by the epidermis. Each growth stage (instar) is designated as either first, second, third, etc, in ascending order of size, or alternatively as A (= Adult), A-I, A-2 etc in descending order. The number of instars is species-specific, from four to nine (Martinsson Reference Martinsson1962; Horne et al. Reference Horne, Cohen, Martens, Holmes and Chivas2002; Smith Reference Smith2025). Ontogenetic development involves, inter alia, the sequential acquisition of appendages and addition and maturation of the sex organs. Embryonic development occurs within what are remarkably hardy eggs. Most ostracods expel their eggs directly into water to develop, but embryo/brood care within the domicilium is known from several major living and fossil taxa (see Horne et al. Reference Horne, Cohen, Martens, Holmes and Chivas2002; Siveter et al. Reference Siveter, Siveter, Sutton and Briggs2007, Reference Siveter, Tanaka, Farrell, Martin, Siveter and Briggs2014, Reference Siveter, Briggs, Siveter and Sutton2015). The first post-embryonic growth stage (nauplius) and subsequent sexually immature juvenile growth stages are succeeded by the last growth stage (adult) which is normally the first and only stage to be fully sexually mature.
Ontogeny of the beyrichioidean Craspedobolbina clavata (Kolmodin, Reference Kolmodin1869), based on Martinsson Reference Martinsson1962, fig. 21. Mulde Brick-clay Member, Halla Formation, Wenlock Series, Silurian, Mulde, Gotland, Sweden.
Sex-related dimorphism of the shell is common in living and fossil ostracods (e.g., Henningsmoen Reference Henningsmoen1965; Vannier et al. Reference Vannier, Siveter and Schallreuter1989; Horne et al. Reference Horne, Cohen, Martens, Holmes and Chivas2002; Ozawa Reference Ozawa and Moriyama2013; Hunt et al. Reference Hunt, Martins, Puckett, Lockwood, Swaddle, Hall and Stedman2017). Some adult and, very rarely, in some species, late juvenile stage specimens (collectively termed heteromorphs) differ morphologically from juvenile and other adult specimens (collectively termed tecnomorphs) of the same species by the development of dimorphic characters of the shell (Fig. 1) involving, for example, carapace size, shape, ornament and/or particular morphological structures. Precocious sexual dimorphism of the carapace and/or some soft parts (e.g., hemipenes, antennae) involving A-1, A-2, A-3 and even A-4 juvenile stages is relatively rare, but is known from both fossil and living species of ostracods; for example, in Myodocopa, Palaeocopida, Platycopida and Podocopida (e.g., see Shaver Reference Shaver1953; Schallreuter Reference Schallreuter1976; Whatley & Stevens Reference Whatley, Stephens, Loffler and Danielopol1977; Hart et al. Reference Hart, Hayek, Clark and Clark1985; Jones Reference Jones1987; Cohen & Morin Reference Cohen and Morin1990; Kamiya Reference Kamiya1992; Tinn & Meidla Reference Tinn and Meidla2003). Some ostracods reproduce asexually: female parthenogenetic populations are known from living species, especially in the freshwater group Darwinulidae (see, e.g., Martens Reference Martens1998; Smith et al. Reference Smith, Kamiya and Horne2006). Parthenogenesis has also been proposed for a few Palaeozoic palaeocopid species (see Section 3).
2. Dimorphism of the shell in major groups of ostracods
Sex-related shell dimorphism in ostracods has been reviewed or featured in many papers, including Ozawa (Reference Ozawa and Moriyama2013) for post-Palaeozoic taxa and Henningsmoen (Reference Henningsmoen1965), Jaanusson (Reference Jaanusson1957, Reference Jaanusson1985), Vannier et al. (Reference Vannier, Siveter and Schallreuter1989), Adamczak (Reference Adamczak1991) and Meidla (Reference Meidla1996) for Palaeozoic species. Dimorphism in ostracods is manifest by spaces of different volumes/configurations in the carapace that in some cases are bounded by dimorphic morphological structures. Dimorphism is essentially either ‘domiciliar’, in which the space that is dimorphic lies within the domicilium, or ‘extradomiciliar’, in which the space in question lies outside the domicilium. Minor ornamental features such as spines may also be dimorphic.
Of the major ostracod taxa, Podocopa and Myodocopa, both of which range from the Ordovician to Recent, display domiciliar shell dimorphism that manifests itself externally in differences in size and shape of the carapace (Fig. 2a–c). In contrast, most Palaeocopida, which are almost exclusively Palaeozoic (e.g., Euychilinoidea, Primitiopsoidea and Hollinoidea), are characterised by extradomiciliar shell dimorphism which involves the addition or modification in one adult of prominent adventral linear ornamental projections and associated spaces external to the domicilium (Fig. 2e–i). Beyrichioidean palaeocopids prominently display domiciliar shell dimorphism, whereby each valve of one of the adults (the presumed female) has extra domiciliary space provided by a special pouch-like structure (crumina) on each valve that opens internally to within the domicilium (Figs 1, 2d, 3, 4c, d, h–k).
Shell dimorphism in some major groups of ostracods. In each dimorphic pair the upper figure is the (assumed) male and the lower figure is the (assumed) female. All lateral views are of left valves except for the images of the female of Xystista graffhami (f, lower) and of the male and female of Tetradella? triloculata (i) which are right valves reversed. An asterisk (*) indicates the approximate limit of the dimorphic region/structure in each female; (a–d) examples of domiciliar dimorphism; (e–i) examples of extradomiciliar dimorphism. (a) Cylindroleberidoidean myodocopid Xenoleberis yamadai (Hiruta, Reference Hiruta1979); Recent, Japan Sea, Oshoro, Hokkaido, Japan. (b) Cytheroidean podocopid Semicytherura sella (Sars, Reference Sars1866); Recent, Oslo Fjord, Norway (after Whittaker Reference Whittaker1974). (c) Cytheroidean podocopid Kuiperiana bathymarina Ayress, Coles & Whatley, Reference Ayress, Coles and Whatley1994; Pleistocene, Tasman Sea (after Ayress et al. Reference Ayress, Coles and Whatley1994). (d) Beyrichioidean palaeocopid Beyrichia clausa Jones & Holl, Reference Jones and Holl1886; Much Wenlock Limestone Formation, Wenlock Series, Silurian, Lincoln Hill, Shropshire, England (after Siveter Reference Siveter, Whittaker and Hart2009). (e) Primitiopsoidean palaeocopid Venzavella costata (Neckaja, Reference Neckaja, Abushik, Ivanova, Kochetkova, Martinova, Netskaya and Rozhdestvenskaya1960); Kaugatuma Regional Stage, Pridoli Series, Silurian, Saaremaa, Estonia (after Siveter & Sarv Reference Siveter and Sarv1991). (f) Triemilomatelline hollinoidean palaeocopid Xystista graffhami (Lundin, Reference Lundin1965); Henryhouse Formation, Ludlow, Series, Silurian, Pontotoc County, Oklahoma, USA (after Lundin & Siveter Reference Lundin and Siveter1985). (g) Tetradellid hollinoidean palaeocopid Harperopsis scripta (Harper, Reference Harper1947); Harnage Shales, Sandbian Stage, Cwms Cottage, near Caer Caradoc, Shropshire, England (after Jones & Siveter Reference Jones and Siveter1983). (h) Euychilinoidean palaeocopid Distobolbina bispinata Schallreuter, Reference Schallreuter1977; Öjlemyrflint erratic boulder, Lummellunds Bruk, Gotland, Sweden, Ordovician (after Schallreuter Reference Schallreuter1977). (i) Tetradellid hollinoidean palaeocopid Tetradella? triloculata Schallreuter, Reference Schallreuter1978; Öjlemyrflint erratic boulder, Ordovician, Gnisvärds, Gotland (after Schallreuter Reference Schallreuter1978). All scale bars represent μm: a, 500; b, 100; c, 100; d, 800; e, 300; f, 400; g, 1000; h, 200; i, 300.
Dimorphism in the beyrichioidean Craspedobolbina clavata (Kolmodin, Reference Kolmodin1869). Mulde Brick-clay Member, Halla Formation, Wenlock Series, Silurian, Mulde, Gotland, Sweden. (a) Male right valve, lateral view (OUMNH PAL-CZ.1021). (b) Female right valve, lateral view (OUMNH PAL-CZ.1022). (c) Transverse section through a female carapace, showing juveniles in the cruminae (from Spjeldaes Reference Spjeldnæs1951, pl. 103, fig. 1). Scale bar (a–c): 400 μm. Repository: Oxford University Museum of Natural History (OUMNH).
Beyrichioideans from the Much Wenlock Limestone Formation, Wenlock Series, Silurian, UK. (a, b, e-g) Ametrobeyrichia schizopyge Siveter, Reference Siveter2022, from Hobbs Ridge, May Hill inlier, Gloucestershire (locality 15b of Siveter Reference Siveter1980). (a, b) Posterior and lateral view stereo-pairs of adult left valve (NHMUK OS6630). (e) Lateral view stereo-pair of probable A-1 left valve of carapace (OUMNH PAL-C.36705). (f) Lateral view stereo-pair of probable A-2 left valve (OUMNH PAL-C.36706). (g) Ventral view of carapace, anterior to the left (NHMUK OS6633). (c, d, h–k) Sleia pauperata (Jones, Reference Jones1869), from Lincoln Hill, near Ironbridge, Shropshire (locality 49c of Siveter Reference Siveter1980). (c, d) Posterior and lateral view stereo-pairs of male left valve (NHMUK OS6400). (h) Ventral view of male carapace, anterior to the left (NHMUK OS6405). (i) Ventral view stereo-pair of female carapace, anterior to the left (NHMUK OS6404). (j, k) Posterior and lateral view stereo-pairs of female left valve (NHMUK OS6401). Repositories: Natural History Museum, London (NHMUK) and Oxford University Museum of Natural History (OUMNH). Scale bar (a–k): 400 μm.
3. Ametrobeyrichia schizopyge: a non-dimorphic beyrichioidean ostracod?
Beyrichioidean ostracods are a major, ubiquitous group of shallow water biostratigraphically important palaeocopids documented from some 180 genera and thousands of species. Most are Silurian or Devonian in age, with just one species known from the Ordovician (Schallreuter Reference Schallreuter1989a, Reference Schallreuter1989b) and a few in the Carboniferous (e.g., Jones Reference Jones1989). Angelin (Reference Angelin1838) was the first not only to recognise that a Silurian form that he named ‘Battus kloedeni n. sp.’ (= Craspedobolbina clavata; Figs 1, 3) is an ostracod but also that it displayed dimorphism of the shell (Spjeldnaes Reference Spjeldnæs1966). Beyrichioidean species are characterised by cruminal domiciliar dimorphism in adults (see, e.g., Hessland Reference Hessland1949; Martinsson Reference Martinsson1962; Siveter Reference Siveter1980, Reference Siveter2022; Adamczak Reference Adamczak1990). The cruminate adult housed juveniles (Fig. 3c) and is presumed to be the female dimorph (Spjeldaes Reference Spjeldnæs1951). Against this background the apparent beyrichioidean Ametrobeyrichia schizopyge Siveter, Reference Siveter2022 (Fig. 4a, b, e–g) from the Silurian of the Welsh basin challenges all records of previously documented beyrichioidean species in seemingly being non-dimorphic by lacking cruminate adults.
Detailed ontogenetic studies of superbly preserved palaeocopid faunas from the Silurian of Gotland, Sweden (Jaanusson & Martinsson Reference Jaanusson and Martinsson1956; Martinsson Reference Martinsson1956) record final growth stage adult sex ratios of 50:50 for four of the species studied (the beyrichioidean C. clavata and two primitiopsoidean and a hollinoidean species) and 30:70 (supposed male:female) for another (primitiopsoidean) species. A. schizopyge is ubiquitous and abundant in the British Silurian. It is known from over 4,100 mostly adult and late growth stage juvenile specimens (Figs 4a, b, e, f, 5) from some 25 localities in mostly the Wenlock (Homerian Coalbrookdale and Much Wenlock Limestone formations) and also Ludlow (Gorstian Lower Elton Formation) series across the Welsh Borderland and English West Midlands (Siveter Reference Siveter2022). In practice, sampling localised marl horizons, weathered debris or shaley bands proved the most successful (and often the only method) to process and obtain abundant and relatively well-preserved ostracods. A. schizopyge is the most common palaeocopid recovered from those localities, but it is represented uniquely and unexpectedly for a supposed beyrichioidean only by non-cruminate specimens. There are other beyrichioidean species also known only from tecnomorphs, but in such cases the total number of specimens recovered is small. Supposed parthenogenesis has also been documented or suggested for a few palaeocopid taxa, including the beyrichioideans Huntonella bransoni Lundin, Reference Lundin1968, Kloedenia leptosoma Martinsson, Reference Martinsson1963 and Kloedenia wilckensiana (Jones, Reference Jones1855) (see Martinsson Reference Martinsson1963) and the primitiopsoidean Clavofabella reticristata (Jones, Reference Jones1888) (see Martinsson Reference Martinsson1956).
Size dispersion of valves of Ametrobeyrichia schizopyge Siveter, Reference Siveter2022 from the Much Wenlock Limestone Formation, Wenlock Series, at Hobbs Ridge, May Hill inlier and Croft Farm, near Malvern (localities 15b and 18 of Siveter Reference Siveter1980).
4. Possible reasons for the non-dimorphic nature of A. schizopyge
4.1. Sexes misinterpreted?
Could the non-cruminate adult of beyrichioidean species be the female and the cruminate forms be the males? As the cruminae of beyrichioideans contain juveniles (Fig. 3c) this interpretation is considered very unlikely, but it nevertheless remains a possibility. Male brood care is known, but only very rarely, from other arthropods; for example, in pycnogonids (King Reference King1973).
4.2. Collecting/sampling failure?
From the at least 25 Silurian localities from which A. schizopyge was recovered, many tens of kilograms of material were sampled, processed and manually picked under a binocular microscope (by David J. S.). It is highly unlikely that sampling, processing or picking issues resulted in a failure to recover cruminate specimens of the species.
4.3. Ecological separation of dimorphs?
Could the dimorphs have lived in separate geographical regions or distinct ecological environments? An analogous case is that of the myodocope ostracod Philomedes globosa in which the females and males inhabit separate water depths and meet only to reproduce. Both Triebel (Reference Triebel1941, p. 362) and Kesling (Reference Kesling1952, p. 266) suggested that some palaeocopid dimorphs may be adapted for life in separate biotopes. That notion found some acceptance with Henningsmoen (Reference Henningsmoen1965, p. 356) but Hessland (Reference Hessland1949, p. 128) considered it doubtful. Moreover, in his comprehensive monographic study of some 120 beyrichioidean species from the Silurian of Gotland Martinsson (Reference Martinsson1962, p. 121) concluded that both sexes and their juvenile stages ‘generally lived together in the same environment’.
Specimens of A. schizopyge are from relatively shallow water shelf facies (Siveter Reference Siveter2022). Perhaps the missing dimorphs lived in the more scarcely sampled deeper basinal environments that existed to the west of the shelf/slope facies in the Welsh Basin in mid-Silurian times? This is considered unlikely, as within the thousands of specimens recovered it might be expected that at least some dimorphs would be preserved together in the same environment.
4.4. Questionable taxonomic assignment?
The notion that the morphology of A. schizopyge is compatible (belongs) with another, non-beyrichioidean palaeocopid group is not sustainable. All valves recovered display the characteristic features of lobate beyrichioidean tecnomorphs (velum, anterior lobe, preadductorial node, syllobium and prenodal and adductorial sulci) and have no morphological feature incompatible with the Beyrichioidea. Plots of the size of specimens of A. schizopyge (e.g., Fig. 5) have not yielded clearly defined growth stages (for possible reasons for this when sampling for Palaeozoic ostracods, such as unsuspectedly collecting across minute chronodemes and/or ecodemes, see Martinsson Reference Martinsson1962, pp. 122, 123), but nevertheless offer no reason to suppose that dimorphism might be reflected merely by size differences. In theory it is possible that A. schizopyge represents a remarkable instance of homeomorphy within Palaeocopida. However, it is the presence and nature of dimorphism that is the key to true affinity of palaeocopid taxa (Swartz Reference Swartz1936; Henningsmoen Reference Henningsmoen1953; Jaanusson Reference Jaanusson1957, Reference Jaanusson1966; Kesling Reference Kesling1969). On balance the evidence strongly suggests that A. schizopyge represents a unique beyrichioidean species, one that has not developed cruminae and cruminal brood care strategy.
4.5. Origin by heterochrony?
Various genetically controlled mechanisms involving the timing and rate of development are normally precisely linked to the eventual size and morphology of an animal, but heterochronic decoupling of mechanisms may result in ‘changes through time in the appearance or rate of development of ancestral characters’ (Gould Reference Gould1977; McNamara Reference McNamara, Briggs and Crowther1990; McKinney & McNamara Reference McKinney and McNamara1991). Heterochronic changes are by nature ‘instantaneous’ and help in understanding the origin of macroevolutionary novelties (Clarkson Reference Clarkson1998). Heterochrony has been suggested to explain morphological aspects of the ontogeny of a few living (e.g., Abe Reference Abe, Hanai, Ikeya and Ishizaki1988; Kamiya Reference Kamiya1992; Tsukagoshi & Kamiya Reference Tsukagoshi and Kamiya1996) and fossil (e.g., Schweitzer et al. Reference Schweitzer, Kaesler and Lohmann1986; Olempska Reference Olempska1989) ostracod species. Some type of paedomorphosis, whereby the complete ‘juvenile’ morphology (or only certain juvenile characters) of the ancestor is retained into the adult of the descendant, resulting in a descendant adult that resembles a juvenile of the ancestral form, may have resulted in the non-dimorphic nature of A. schizopyge. The valve morphology of A. schizopyge bears general similarity to tecnomorphs of European Silurian dimorphic beyrichiine beyrichioideans such as species of Plicibeyrichia, Gannibeyrichia and Navibeyrichia (all Martinsson Reference Martinsson1962) and Pseudobeyrichia cristata Copeland, Reference Copeland1989 from Canada. A. schizopyge especially resembles tecnomorphs of the amphitoxotidine beyrichioidean Sleia Martinsson Reference Martinsson1962 from which it differs only in minor details of syllobial morphology and by the lack of a characteristic tubercle dorsally on the adductorial sulcus (Fig. 4a, b, e–g; cf. Fig. 4a, d, h). Of six species of Sleia in the Silurian of Britain four occur at Wenlock Series localities with A. schizopyge (Siveter Reference Siveter2022), including the morphologically closely similar Sleia pauperata (Jones, Reference Jones1869) whose adults are of similar size to those of A. schizopyge (Fig. 4c, d, h–k). Some form of paedomorphosis acting in a beyrichioidean morphologically similar to a Sleia species may be the evolutionary origin of A. schizopyge.
5. Conclusions
Beyrichioidean ostracods are known abundantly worldwide from hundreds of Palaeozoic genera. Each is characterised by a distinctive well-defined shell dimorphism in which the supposed female of the species develops a pronounced brood pouch (crumina) on each valve. A. schizopyge, a ubiquitous Silurian ostracod species from the UK, fundamentally challenges the definition of the group. Known only from juveniles and supposed adults of like morphology it is, ostensibly, a unique, non-dimorphic beyrichioidean species. Its apparent non-dimorphic nature may have resulted from a heterochronic mechanism. Seemingly not all beyrichioideans had cruminal brood care strategy.
Acknowledgements
We thank Dr Leon Hicks and Professor Mark Williams (University of Leicester) for scanning electron microscope work. We are grateful to Dr Vincent Perrier (University of Lyon) and one other referee for comments on the manuscript.
Competing interests
The authors declare no competing interests.
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