BULLETIN OF MARINE SCIENCE. 57(2): 516-526. 1995 CORAL REEF PAPER EVOLUTION OF LIFE-HISTORY PATTERNS IN THREE GENERA OF SPINY LOBSTERS David E. Pollock ABSTRACT The life-history patterns and probable evolutionary pathways of three extant genera of spiny lobsters are compared. The deep-water genus Palinurus and the shallow-water genus PanuLirus are members of the Stridentes (sound-producing) lineage, while the cool-temperate shallow-water genus Jasus belongs to the Silentes group. The Stridentes and Silentes lineages evolved independently for over 150 million years, yet species of the two lineages still share a number of common characteristics, including a leng-lived phyllosoma larval phase and remarkably similar adult morphology. Species of the two shallow-water genera, Jasus and Panulirus. differ from each other, and from the deeper-water Palinurus species, in certain aspects of reproduction. A post-Miocene shift from deep to shallow waters in thc former two genera has apparently been accompanied by changes in mechanisms of fertilization and in- creased egg production. These adaptations are likely to have evolved in response to higher natural mortality rates and greater environmental variability in shallower waters. Three genera of spiny lobsters, Jasus, Palinurus and Panulirus are the subject of this paper. The genus Palinurus has a fossil record dating to the Cretaceous (Glaessner, 1969), and extant species of Palinurus are considered to be more 'primitive' than species of the genus Panulirus, which is considered to have a more recent post-Miocene origin (George and Main, 1967). Both of these genera have been placed in a group of spiny lobsters known as the Stridentes (sound- producers) by George and Main (1967). This group also includes a number of less well-known genera such as Linuparus, Justitia, Puerulus and Palinustus, all of which are relatively deep-water forms. The genus Jasus was placed by George and Main (1967) in a separate group, the Silentes, which also includes the extant genus Projasus, a relatively deep- water genus. These authors considered that the Silentes group split off the ances- tral Pemphicidae stock more than 150 million years ago [see Fig. 1, extracted from George and Main (1967)]. In contrast to the Stridentes, the Silentes group have no sound-producing stridulatory apparatus. Despite the fact that the two lineages, Stridentes and Silentes apparently evolved independently from each other during the course of hundreds of millions of years, extant species within these two groups share a large number of char- acteristics, in terms of morphology, behavior and certain life history patterns. Life history characteristics of the three genera of spiny lobsters are compared in this paper, and possible selective advantages of particular features are discussed. EVOLUTIONARY HISTORY AND PRESENT-DAY DISTRIBUTIONS Although the fossil record of most palinurids is scanty, some limited infor- mation is available to help sketch the likely evolutionary backgrounds of each of the three genera. A brief summary of the probable evolutionary history of each genus is presented below: Jasus.- This genus comprises seven extant species, of which six (the Jasus la- landii group) occupy a shallow-water, cool-temperate, circumglobal, southern hemisphere distribution, mainly between latitudes 27°-45° south. A seventh, very 516 POLLOCK: EVOLUTION IN SPINY LOBSTERS 517 SILENTES STRIDENTES 2 5 25 55 65 135 190 225 Figure 1. Diagram of postulated palinurid evolution redrawn from George and Main (1967). Fossil records are indicated in black, probable records are dotted. Scale on the right is millions of years B.P. large and highly fecund species, J. verreauxi, is endemic to the subtropical east coast of Australia and northern New Zealand. Breeding populations of J. verreauxi are confined to latitudes north of 33°S in Australia and to the extreme north of North Island, New Zealand (MacIntyre, 1967; Booth, 1986). J. verreauxi is mor- phologically very similar to an extinct form, J. jiemingi, a Miocene species which was found as a fossil in central New Zealand, dated at about 20 million years old (George, 1969). George (1969) considered that J. jiemingi may have been an ancestral Tertiary form which occupied the western Pacific region during earlier times when water temperatures were warmer than during the Quaternary. Pollock (1990) suggested that a late Miocene radiation of species of the J. lalandii group took place when the opening of the Drake Passage and the development of the circum antarctic current allowed teleplanic phyllosoma larvae of Jasus to enter the south Atlantic and South Indian Oceans, where colonization of suitable cool water island and mainland habitats took place. Repeated local extinctions and recolo- nisations of island habitats were probably a feature of Pleistocene glaciaVinter- glacial oscillations. In modern times, the phyllosoma larvae of extant Jasus spe- cies appear to be retained within the eddies and gyres of the large-scale anticy- 518 BULLETIN OF MARINE SCIENCE, VOL. 57, NO.2, 1995 clonic circulation systems of the southern ocean basins, implying an extended larval duration of years rather than a few months, and suggesting a well-developed ability of phyllosoma larvae to delay metamorphosis into the swimming puerulus stage (Pollock, 1990). Palinurus.-Five extant species of this moderately deep-water genus exist. P. elephas occurs in the Mediterranean Sea and eastern North Atlantic Ocean. This species may be a relict of an ancestral form, P. vulgaris, fossils of which have been recorded from Upper Cretaceous sediments in the same region (Glaessner, 1969), an area which at that time would have comprised the Tethys Sea, a seaway linking the Indian and Atlantic Ocean in pre-Miocene times (Kennett, 1982). The four other extant species are: P. mauretanicus (N.W. African coast); P. charlestoni (Cape Verde Islands); P. delagoae (S. Madagascar and the south-east coast of southern Africa), and P. gilchristi (south coast of South Africa). All five species are fairly similar morphologically but are distinguished by characteristic differences in the grooves on the abdominal somites and a few other minor mor- phological features (Holthuis, 1991). Panulirus.-This relatively recent (post-Miocene) genus of spiny lobsters com- prises some 20 extant species, occupying subtropical and tropical shallow-water habitats worldwide. George and Main (1967) considered that the genus Panulirus emerged towards the end of the Pliocene epoch, some 2 to 3 million years ago. Certain species of the genus have lost all or some of the exopods of the 2nd and 3rd maxillipeds, and George and Main (1967) divided the species into four groups, based on morphological similarities in the exopod condition of the maxillipeds. Those species with the most reduced exopods were regarded as the most advanced forms-they comprise the Indo-West Pacific species P. ornatus, P. homarus, P. stimpsoni and the east Pacific species P. gracilis and P. inflatus. At the other extreme, species with the most intact exopods, considered to be the most primitive condition, included P. argus (west Atlantic), P. interruptus (east Pacific) and the five species of the P. japonicus group (Indo-West Pacific). George and Main (1967), and later Pollock (1992) described possible mecha- nisms involved in the Pleistocene species radiation of several Panulirus species, suggesting that oceanographic barriers to larval dispersal and gene flow amongst widespread populations of ancestral species ultimately led to allopatric speciation in various ocean basins. Species of this genus have a number of adaptations which are well-suited for survival in the highly variable shallow-water environments of the Quaternary oceans. LIFE HISTORY PATTERNS Egg Size, Brood Size and Lifetime Egg Production.-Table I compares a number of life history parameters associated with egg and larval production in the three genera. In the two shallow-water genera, Jasus and Panulirus, high lifetime egg production (E/R) is achieved in different ways, as discussed by Pollock and Mel- ville-Smith (1993). In Jasus species, annual broods are moderate in size with eggs intermediate in size between the other two genera (Table 1). However, a lengthy adult lifespan coupled with relatively low natural mortality rates allows lifetime egg production of the order of a million eggs per female. In Panulirus species, high egg production (E/R) is achieved through the repet- itive production of large broods of small eggs, produced throughout a relatively short adult lifespan (Pollock and Melville-Smith, 1993). This explains how E/R POLLOCK: EVOLUTION IN SPINY LOBSTERS 519 Table I. Comparison of some life history parameters in Jasus, Palinurus and Panulirus species Character lusus Palinurus Panu/irus EIR I X 106 0.5 X 106 1.2 X 106 (Pollock, ]987) (Pollock and Me]ville (Pollock and Me]ville Smith, 1993) Smith, 1993) Egg size index* 300-500 200 400-800 (Pollock, ]991) (Pollock and Me]ville (Pollock and Melville Smith, 1993) Smith, 1993) Brood size (at 90 125,000-195,000 80,000-] 10,000 300,000-550,000 mm CL) (Pollock, 1991) (Pollock and Melville (Berry, 1971; Phillips et Smith, 1993) aI., 1980) Puerulus size (CL 10-12 10 6-8 mm) (Pollock, 1991) (Bouvier, 1913; Kittaka (Sweat, ]968; Phillips et 1988b) aI., 1977; Serfling and Ford, 1975; Berry, 197]) No. of larva] in- 15-17 8-9 15-25 stars (Kittaka, 1988a) (Kittaka, 1988b) (Braine et aI., ]979; John- son and Knight, ]966) No. of larva] 1]-13 9-11 stages (Lazarus, ]967; Sil- (Johnson, 197]; Inoue, berbauer, ]971; 1978; Braine et aI., Kittaka, 1988a) ]979) " No. of eggs per g body weight: an index which is inversely proportional to egg size. - No information. of P. homarus may be similar to that of J. lalandii, despite the much shorter lifespan of Panulirus species in subtropical and tropical waters, where natural mortality rates due to predation are also much higher than in the cool temperate regions occupied by most Jasus species.